11 Ustilaginomycotina

Begerow, D.; Schäfer, A. M.; Kellner, R.; Yurkov, A.; Kemler, M.; Oberwinkler, F.; Bauer, R.

doi:10.1007/978-3-642-55318-9_11

D. Begerow⁴,
A. M. Schäfer⁴,
R. Kellner⁵,
A. Yurkov⁶,
M. Kemler⁷,
F. Oberwinkler⁸ &
…
R. Bauer⁸

Part of the book series: The Mycota ((MYCOTA,volume 7A))

3133 Accesses
32 Citations

Abstract

Ustilaginomycotina represents one of three subphyla of the Basidiomycota, comprising 10 orders, 26 families, and 121 genera, with more than 1,700 species in total. Whereas most of the species are plant parasites with a biphasic life cycle and largely strong host preference, some species are recognized solely from their anamorphic phase. In addition, Ustilaginomycotina contains some lineages that parasitize hosts outside the plant kingdom, for example, the mammal-pathogenic genus Malassezia. In this chapter we summarize the most recent systematic studies of Ustilaginomycotina by highlighting the unique characters of monophyletic lineages. Furthermore, evolutionary trends are discussed.

Access provided by Autonomous University of Puebla. Download chapter PDF

3 Pezizomycotina: Sordariomycetes and Leotiomycetes

5 Pezizomycotina: Eurotiomycetes

6 Pezizomycotina: Dothideomycetes and Arthoniomycetes

Keywords

These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

I. Introduction

Ustilaginomycotina comprises 115 genera with more than 1,700 species and represents one of the three subphyla of the Basidiomycota (Bauer et al. 2006; Begerow et al. 1997; Hibbett et al. 2007; Swann and Taylor 1993). They harbour mostly plant parasites (Fig. 11.1a–p) that are restricted to the geographic distribution of their hosts, encompassing tropical, temperate, and Arctic regions (Vánky 2012).

Well-known genera in Ustilaginomycotina are Ustilago and Tilletia , which contain economically important species such as karnal bunt of wheat, loose smut of barley, and corn smut (Thomas 1989; Trione 1982; Valverde et al. 1995). In some cases where yield loss is minimal, contamination of Tilletia smut spores in grain can be subjected to quarantine regulations with economic implications and restrictions to international trade (Carris et al. 2006; Pascoe et al. 2005). Corn smut Ustilago maydis (DC.) Corda generally infects 2–5 % of plants in a corn field, although under certain conditions it can infect up to 80 % (Christensen 1963). While considered a plant pathogen in some parts of the world, the galls of U. maydis are appreciated as a delicacy in Mesoamerican cooking (Juarez-Montiel et al. 2011; Zepeda 2006). Besides the well-known species on crops, a huge diversity of plant parasites exist that either induce a typical smut syndrome (Fig. 11.1i–p) or present inconspicuous infections like members of Entylomatales (Fig. 11.1b), Exobasidiales (Fig. 11.1c–e), or Microstromatales (Fig. 11.1h). In addition, Ustilaginomycotina harbours some ecologically variable anamorphic lineages such as Malassezia , which colonizes human and animal skin (Begerow et al. 2000, 2006).

Among the morphologically and ecologically diverse species of Ustilaginomycotina , U. maydis became a model organism for studying the interaction of specific plant parasites with their hosts. Using a variety of genetic tools, it has been shown that mating is an essential prerequisite to plant infection (Kahmann and Kämper 2004). U. maydis was one of the first fungal genomes sequenced, which advanced the knowledge of fungal physiology, such as the importance of secreted proteins in signaling (Brefort et al. 2009; Kämper et al. 2006). Thus, Ustilaginomycotina is a highly valuable group for comparative genomic studies in fungal pathogens and for illuminating the evolution and functionality of host–parasite interactions (Kellner et al. 2011; Schirawski et al. 2010; Xu et al. 2007).

A. Diagnosis and Evidence for Monophyletic Origin

The Ustilaginomycotina have a distinctive cell wall composition with a dominance of glucose and an absence of xylose, which separates them from the Pucciniomycotina and Agaricomycotina (Prillinger et al. 1990, 1993). They share the type B secondary structure of 5S ribosomal RNA (rRNA) with the Agaricomycotina (Gottschalk and Blanz 1985) and the lack of parenthesomes (i.e. multilayered endoplasmic reticulum elements at the septal pores) with the Pucciniomycotina (Bauer et al. 1997, 2006). Important synapomorphies for the Ustilaginomycotina are membranous pore caps and the presence of a characteristic host–parasite interaction zone that results from fungal exocytosis of primary interactive vesicles (Bauer et al. 1997).

Sequence analyses support the monophyly of the Ustilaginomycotina as defined earlier but with varying statistical support in different studies. Whereas the monophyly of Tilletia caries (DC.) L. & C. Tul., Ustilago hordei (Pers.) Lagerh., and U. maydis had high bootstrap support with small subunit (SSU) rDNA sequence analyses (Bauer et al. 2006; Swann and Taylor 1993, 1995), the bootstrap values for the Ustilaginomycotina were lower when analysed with large subunit (LSU) rDNA sequences and increased taxon sampling (Begerow et al. 1997, 2000). In particular, bootstrap support for the Ustilaginomycotina was sensitive to the inclusion or exclusion of Entorrhiza sequences in the LSU data set; after several analyses and varying interpretations Entorrhiza was excluded from the Ustilaginomycotina (Hibbett et al. 2007; Matheny et al. 2006). To date, the phylogenetic position of Entorrhiza remains unresolved.

B. Smut Fungi Syndrome in Other Fungal Groups

Like the terms agaric, polypore, and lichen, for example, the term smut fungus circumscribes the organization and life strategy of a fungus (cf. Fig. 11.1a–p) but does not represent common ancestry. Hence, smut fungi are non- monophyletic when based on the presence of a powdery spore mass. Most smut fungi are in the Ustilaginomycotina . Other smut fungi, in the Microbotryales , are members of the Pucciniomycotina (Bauer et al. 2006; Begerow et al. 1997; see Aime et al. 2014). In contrast to the Ustilaginomycotina , available data indicate that the microbotryaceous taxa Aurantiosporium , Bauerago , Fulvisporium , Liroa , Microbotryum , Sphacelotheca , Ustilentyloma, and Zundeliomyces have a type A 5S rRNA secondary structure (Gottschalk and Blanz 1985; Müller 1989), mannose as the major cell wall carbohydrate (Prillinger et al. 1991, 1993), and cellular interactions without primary interactive vesicles (Bauer et al. 1997), all of which are synapomorphies of the Pucciniomycotina . Morphologically, they are distinguishable from the phragmobasidiate members of Ustilaginomycotina by the lack of intracellular hyphae or haustoria (Bauer et al. 1997). Grouping the Microbotryales within the Pucciniomycotina rather than the Ustilaginomycotina is also supported by sequence analyses (Bauer et al. 2006; Begerow et al. 1997; Swann and Taylor 1995). However, there are significant convergences between the microbotryaceous and ustilaginomycetous phragmobasidiate smut fungi. Certain taxa of both groups are similar with respect to soral morphology, teliosporogenesis, life cycle, basidial morphology, and host range (Bauer et al. 1997, 2006).

As stated previously, Entorrhiza has been excluded from the Ustilaginomycotina mainly based on molecular phylogenetic analyses (Hibbett et al. 2007). Early studies using a smaller number of taxa placed Entorrhiza species basal to other Ustilaginomycotina with low bootstrap support (Begerow et al. 1997). Later studies questioned this position, and, depending on species sampling and outgroup selection, the position of Entorrhiza remains more or less unresolved (Begerow et al. 2006; Matheny et al. 2006). As long as a thorough multigene analysis is lacking, we follow the concept of Hibbett et al. (2007) and exclude Entorrhiza from the Ustilaginomycotina .

Interestingly, even non-basidiomycetous fungi can cause diseases with the formation of thick-walled propagules convergent to those of smut fungi. Species of Schroeteria Winter, for example, look superficially similar to Ustilaginomycotina (Vánky 1981) but belong to the Ascomycota (Nagler et al. 1989). Leaf spots similar to sori of Entyloma can be formed by representatives of the Protomycetales (Reddy and Kramer 1975), which belong to the Taphrinomycotina (Sugiyama et al. 2006; see Kurtzman and Sugiyama (2014), Chap. 1 Vol. VII, Part B) and produce ascospores in their synasci (Preece and Hicks 2001).

C. Hosts and Their Role in Species Definition

The Ustilaginomycotina , unlike the Pucciniomycotina and Agaricomycotina , generally are ecologically well characterized by parasitism . Besides some anamorphic taxa, which will be discussed in more detail later, all members of Ustilaginomycotina are plant parasites . Aside from Exoteliospora on ferns (Bauer et al. 1999b), two species of Melaniella on spike mosses (Bauer et al. 1999a), and two species of Uleiella on conifers (Butin and Peredo 1986; Schröter 1894), all other plant parasitic members of Ustilaginomycotina parasitize angiosperms with a high proportion of species on monocots , especially Poaceae and Cyperaceae . The majority of the roughly 1,710 species occur on Poaceae (45 %) or on Cyperaceae (13 %) . The 121 ustilaginomycetous genera occurring on angiosperms include 72 genera that are exclusively found on monocots and 31 exclusively on dicots (mainly eudicots); 4 comprise species that parasitize both monocots and dicots. The genera found exlusively on monocots occur mainly on Poaceae (22) and on Cyperaceae (20, see below). Concerning the hosts, there are two remarkable points. (1) With a few exceptions, the teliospore-forming species of Ustilaginomycotina parasitize nonwoody herbs, whereas those without teliospores prefer woody trees or bushes. However, almost all species sporulate on parenchymatic tissues of the hosts. (2) Two of the angiosperm families with the highest number of species, the Orchidaceae with ca. 20,000 species and the Poaceae with ca. 10,000 species, play quite different roles for the Ustilaginomycotina . There are no known smut species on Orchidaceae, while the Poaceae are the most important host family of Ustilaginomycotina . Grass smuts have obviously adapted to the ecology of their host group by wind-borne teliospores or basidiospores and are thereby able to infect hosts that often occur in extensive, but often disconnected, host populations.

Host range used to play an important role in species definition. Many species, for instance in the genera Entyloma , Melanotaenium, and Urocystis (Vánky 1994), have few defining morphological characters, which, until the advent of ultrastructural techniques, were mainly limited to spore ornamentation and spore size. Therefore, host information has long been used in the delimitation of smut species as an additional defining characteristic. Different authors gave host specificity different emphases. Savile (1947), for instance, accepted only two species in Entyloma and lumped many already described species into these, whereas Vánky (2012) applied a narrower species definition and recognized 163 species based on spore morphology and host. Besides morphological and ecological concepts, phylogenetic species definitions have attracted much attention in recent years [for a review see Cai et al. (2011)], and phylogenetic approaches have in general confirmed the latter position (e.g. Begerow et al. 2002, 2004). These studies question the roles of host interaction and host range in maintaining species integrity of smuts. The species concept of smut fungi is especially perplexing because not only can closely related species [e.g. Tilletia controversa J.G. Kühn and T. caries (DC.) Tul. & C. Tul] hybridize under laboratory conditions (Trail and Mills 1990), but hybridization can even be observed between species that had their own evolutionary trajectory for millions of years (Kellner et al. 2011). It is unknown how gene flow is prevented in nature and how species integrity is maintained for the Ustilaginomycotina , but in microbotryaceous smuts, hybrid inviability was shown to select against hybrids (De Vienne et al. 2009).

In U. maydis, sorus formation is initiated by a combination of parasite and host effectors . To develop teliospores , U. maydis specifically alters plant expression, initiating different expression profiles in different host tissues (Skibbe et al. 2010). These experiments demonstrated that the interaction between smuts and their hosts is extremely tight at the molecular level, which suggests that there are strong factors in maintaining boundaries between parasite species. Thus, species concepts incorporating host information, as applied by smut fungal taxonomists for the last century, have a biological basis, which could explain such narrow host ranges in smut fungi (Cai et al. 2011).

II. Life Cycle

Species of Ustilaginomycotina share a similar dimorphic life cycle comprised of a saprobic haploid phase and a parasitic dikaryotic phase (Fig. 11.2) (Brefeld 1883; de Bary 1884; Sampson 1939). The haploid phase is initiated usually by the formation of basidiospores following meiosis of the diploid nucleus in the basidium and ends with the conjugation of compatible haploid cells to produce dikaryotic, infectious hyphae. The dikaryotic phase ultimately results in the production of probasidia (i.e. often teliospores) or basidia (Fig. 11.3a–o).

Almost all Ustilaginomycotina sporulate on or in parenchymatic tissues of their hosts. In the majority of the Ustilaginomycotina , the young basidium becomes thick-walled and at maturity separates from the sorus to function as a dispersal agent, the teliospore. Teliospores are usually the most conspicuous stage in a smut’s life cycle, representing the smut syndrome (cf. Fig. 11.1a–p). Most of the Ustilaginomycotina are dimorphic and produce a yeast or yeast-like stage in the haploid phase and form hyphae during the parasitic phase. However, there are several variations from this generalized life cycle, e.g. the occurrence of homothallism in Anthracoidea (Kukkonen and Raudaskoski 1964) and Exobasidium (Sundström 1964), the lack of teliospores in the Microstromatales , Exobasidiales and Ceraceosorales (Begerow et al. 2001, 2002, 2006), or even the switch to a complete anamorphic life style as assumed for Malassezia (Boekhout et al. 2010) and other anamorphic genera.

A. Saprobic Phase

Members of Ustilaginomycotina can survive outside their hosts during a free-living asexual state, the saprobic phase . Many representatives are readily obtained from nature as predominantly unicellular budding states, called yeasts or sporidia, e.g. species in Ustilago , Microstroma, and Malassezia (Begerow et al. 2000). Additionally, some smut fungi (e.g. Exobasidium and Georgefischeria ) produce ballistospores to actively discharge basidiospores or secondary spores (Begerow et al. 2000). Hyphal growth is present in the saprobic phase of some members of Ustilaginomycotina ; in many cases, a clear distinction between unicellular, yeast-like, pseudohyphal, and hyphal proliferation is impossible because budding cells (blastoconidia) often originate from hyphae and vice versa. This yeast–hyphal dimorphism occurs in many lineages of the Basidiomycota and might be a distinctive feature of parasitic lineages (Sampaio 2004).

In members of Ustilaginomycotina , yeast and yeast-like states are known from five orders: Ustilaginales , Entylomatales , Exobasidiales , Georgefischeriales, and Microstromatales (Begerow et al. 2000; Boekhout et al. 2011; Sampaio 2004). In the order Urocystidales , saprobic yeast-like growth of secondary sporidia was observed in some Thecaphora species (Vánky et al. 2008a) and in Urocystis cepulae Frost (Whitehead 1921). No such yeast states are known from the Doassansiales and Tilletiales .

Multiplication and propagation as yeast and yeast-like states are likely to be advantageous for survival and dispersal, and actually some taxa are known from their asexual states only, namely Pseudozyma , Tilletiopsis , Sympodiomycopsis , Meira , Acaromyces , Jaminaea , Malassezia, and probably Quambalaria . Members of these genera have mostly been isolated from various substrates during analyses of yeast communities in specific habitats (de Beer et al. 2006; Kurtzman et al. 2011).

Despite the economic relevance of smut infections caused by Ustilago , Quambalaria, and many others, and the rather high frequency of occurrence, little is known about the distribution of free-living yeast states. Assimilation tests , which are routinely performed for fungi historically treated as yeasts (Pseudozyma , Sympodiomycopsis , Rhodotorula ), reveal the abilities of free-living states of Ustilaginomycotina to utilize a broad spectrum of plant-related carbohydrates, like sucrose, cellobiose, trehalose, l-arabinose, d-xylose, and some polyols (Kurtzman et al. 2011). Additionally, the capability of species of Ustilaginales (Sporisorium , Ustilago , Farysia , Farysyzyma, Pseudozyma ), Entylomatales (Entyloma , Tilletiopsis ), and Microstromatales (Sympodiomycopsis , Rhodotorula ) to break down and assimilate low-weight aromatic molecules has been demonstrated (Sampaio 1999). Most of the tested cultures were able to use intermediates of lignin degradation, such as protocatechuic, p-coumaric acid, vanillic, and p-hydroxybenzoic acids (Sampaio 1999; Subba Rao et al. 1971). This adaptation seems especially interesting for dimorphic plant parasites because it might enable active degradation of cell walls , thereby allowing survival on decaying plant material. Besides the use of ligno-cellulosic derivates, the utilization of several non-conventional carbon sources of plant origin by species of Ustilaginomycotina has been reported, e.g. Tilletiopsis washingtonensis Nyland assimilates diverse volatile organic carbon (VOC) sources present in ripe apples (Vishniac et al. 1997). Interestingly, one component of VOC (butyl acetate), successfully utilized by T. washingtonensis, stimulates germination of grey mould (Botrytis cinerea Pers.) conidia, and the consumption of gaseous carbon products by T. washingtonensis decreases the development of moulds on apples (Filonow 2001). Members of Entylomatales display growth on gentisic acid (Sampaio 1999), a compound involved in regulating the defense responses of plants (Bellés et al. 2006). Members of Entylomatales and Microstromatales are able to grow on gallic acid (Sampaio 1999), a widely distributed tannin often accumulated in substantial quantities in plant material (Haslam and Cai 1994). Furthermore, the capability of some species of Tilletiopsis , Pseudozyma , and Ustilago to secrete enzymes, such as lipase, amylase, glucoamylase, cutinase, protease, pectinase, and xylanase, has been reported (Boekhout et al. 2006, 2011; Geiser et al. 2013; Trindade et al. 2002; Urquhart and Punja 2002).

Several interesting physiological adaptations seem to facilitate saprobic growth and survival in natural habitats. Cold tolerance is a common trait among basidiomycetous yeasts, which successfully colonize extremely cold habitats , including glaciers (Branda et al. 2010) and high-altitude regions (Connell et al. 2008; Vishniac 2006). Low temperatures also favour the development of various species of Tilletiopsis and anamorphs of Entyloma (Boekhout et al. 2006 and references therein). Extensive growth of Tilletiopsis spp. on apple surfaces under low oxygen concentration was reported recently (Boekhout et al. 2006). Although it is not yet clear whether this ability provides any advantage in colonizing plant substrates, several yeasts (e.g. Meira spp., Pseudozyma spp.) were reported from inside plant tissues (Abdel-Motaal et al. 2009; Gerson et al. 2008; Paz et al. 2007; Posada and Vega 2005; Takahashi et al. 2011; Tanaka et al. 2008; Yasuda et al. 2006).

The secretion of antibiotic compounds, killer toxins (proteins), and glycolipids could give yeasts a competitive advantage against other microorganisms . Glycolipids are modified long-chain fatty acids that are active against diverse groups of fungi (Golubev 2007; Mimee et al. 2005; Teichmann et al. 2007), bacteria (Kitamoto et al. 1993), and insects (Gerson et al. 2008). Antagonistic reactions towards other fungi were reported for Acaromyces ingoldii Boekhout, Scorzetti, Gerson & Sztejnb. and several species of the genera Meira , Pseudozyma , Tilletiopsis, and Sympodiomycopsis (Boekhout 2011; Gerson et al. 2008; Golubev 2006, 2007; Golubev et al. 2008). Consequently, some Ustilaginomycotina yeast species might even have evolved a mycoparasitic life style, as has been suggested for T. pallescens Gokhale, which was repeatedly isolated from basidiocarps of other fungi (Boekhout 2011). Recently, two asexual genera, Meira and Acaromyces , were found to cause the mortality of citrus mite pests (Paz et al. 2007). Although these fungi grew on mite cadavers, the capability of cell-free extracts from cultures to kill mites suggests the toxic nature of fungal secretions rather than a parasitic life style. Interestingly, cell-free extracts effectively suppressed the growth of several plant pathogens, including moulds, mildew, and soil-borne fungi (Kushnir et al. 2011).

It is not surprising that saprobic states of Ustilaginomycotina were found on different plant-related substrates (Begerow et al. 2000; Fonseca and Inácio 2006; Sampaio 2004). In some cases saprobic and parasitic states co-exist in the same natural habitat ; however, a considerable number of species were isolated from distinct substrates (water, nectar, and fruits) or from plants totally unrelated to the known hosts. Yeasts of the genus Farysizyma , probably the anamorphic stage of Farysia , which parasitizes Cyperaceae , have been recovered from leaves of unrelated plant species of Bromeliaceae and Cistaceae, strawberry fruits, and nectar (Inácio et al. 2008). Other substrates, i.e. water, fruit pulps and flowers, also yielded saprobic states of Ustilaginomycotina (Fell et al. 2011; Inácio et al. 2008; Liou et al. 2009; Seo et al. 2007; Trindade et al. 2002; Wang et al. 2006). Although some authors reported the isolation of Pseudozyma yeasts from clinical samples, invasive disease caused by these fungi are very unusual in humans (Lin et al. 2008; Sugita et al. 2003), and only yeasts of the genus Malassezia are considered to be part of the normal skin mycobiota of warm-blooded vertebrates (Findley et al. 2013) . However, in many circumstances they have been reported to cause various types of skin diseases like pityriasis versicolor, seborrheic dermatitis, and folliculitis (Boekhout et al. 2010).

Finally, the dual nomenclature introduced for anamorphic strains and species remains problematic because some of them represent the anamorphic stage of a well-known teleomorph (Begerow et al. 2000; de Beer et al. 2006). The application of the new rules provided by the Melbourne Code will allow phylogenetic species recognition, and it is hoped that some of the systematic problems will be resolved in the near future (Hawksworth 2011; Hawksworth et al. 2011), but the integration of anamorphic and teleomorphic systematics and nomenclature remains a challenge.

B. Parasitic Phase

The parasitic phase in Ustilaginomycotina is initiated by the mating process, which induces a morphological and physiological transition from saprophytic yeast cells to biotrophic filaments (Fig. 11.2) (Kahmann and Kämper 2004; Kellner et al. 2011; Snetselaar and Mims 1992). The genetic and developmental basis of the infection process and the host–parasite interaction have been studied best in the model organism U. maydis and will not be reviewed in detail [for a more detailed view see Brefort et al. (2009), Kahmann and Kämper (2004) and Vollmeister et al. (2012)]. To form an infectious dikaryotic hypha, two compatible haploid sporidia must recognize each other and fuse. In U. maydis the cell cycle arrests during mating until after host penetration (Garcia-Muse et al. 2003). Penetration is achieved via non-melanized appressoria at the tip of elongated dikaryotic cells and might additionally be aided by the secretion of lytic enzymes (Schirawski et al. 2005).

The subsequent steps of infection depend on the ability of the fungus to establish an intimate interaction with its specific host (Fig. 11.4a–e). This is mediated by the vesicle -based exocytosis (Bauer et al. 1997) of secreted effector proteins that interfere with plant defenses (Brefort et al. 2009) and host-specific metabolic processes (Djamei et al. 2011). Depending on the respective ustilaginomycetous group, hyphae grow and proliferate either only intercellularly or both intercellularly and intracellularly (Fig. 11.4a–e) (Bauer et al. 1997). Intracellular hyphae are tightly surrounded by the plant plasma membrane and develop a characteristic vesicular matrix through the accumulation of secreted deposits (Bauer et al. 1997). Members of Doassansiales , Entylomatales, and Exobasidiales develop a characteristic interaction apparatus (Fig. 11.4b–d), while other groups of Ustilaginomycotina interact with their host either via small evagination zones (Fig. 11.4a) or along the whole hyphae (Fig. 11.4e). These hyphae are usually not restricted to specific entrance or exit sites of host cells and, therefore, can passage from cell to cell (Bauer et al. 1997). In the Ustilaginaceae, hyphae grow directly to plant vascular bundle cells and proliferate throughout the host in close proximity to the vascular system until they reach their sporulation sites (Doehlemann et al. 2009). During proliferation, fungal hyphae branch and undergo mitosis and septation (cf. Fig. 11.5a–e). Members of Doassansiales , Ustilaginales, and some species of Exobasidium develop clamps to coordinate the synchronized division of the two nuclei. In U. maydis clamp primordia are formed at the tip of the growing hyphae (Scherer et al. 2006). However, clamp-like structures are observed in many species of Ustilaginomycotina . Whilst some clamps give rise to hyphal branches, others seem to correspond to fusion bridges (Fischer and Holton 1957), which ensure the migration of nuclei rather than coordinating dikaryotic mitoses.

Proliferation in the host is followed either by the direct formation of basidia, as observed in Microstomatales , Exobasidiales, and Ceraceosorales (Fig. 11.3l–o), or by the production of teliospores , which are clustered in sori (e.g. Fig. 11.1b, c, f, j–p). Sporogenesis of teliospores often occurs in distinct organs of a plant, including roots, stems, leaves, inflorescences, anthers, ovaries, and seeds (Fig. 11.1) (Vánky 2012). In this process biotrophic hyphae aggregate, septate, and finally differentiate into teliospores. However, teliospore formation is variable among members of Ustilaginomycotina, and propagation units range from single spores to large spore balls, which may or may not include sterile cells (Piepenbring et al. 1998). This variability can even be observed between closely related species, e.g. in Urocystis and Thecaphora (Vánky et al. 2008a). In Ustilago nearly all hyphae disarticulate and form teliospores in a matrix resulting from gelatinization of hyphal cell walls (Snetselaar and Mims 1994), whereas teliospores in Rhamphospora are formed terminally and without recognizable gelatinization (Piepenbring et al. 1998). Usually, sporogenesis occurs intercellularly either in preformed intercellular spaces or in cavities of disintegrated host cells (Luttrell 1987). The release of teliospores does not depend on living host tissue since Schizonella and some species of Ustilago sporulate within disintegrated host tissues, and species of Clintamra , Exoteliospora, and Orphanomyces even develop their teliospores externally to the host tissue (Piepenbring et al. 1998; Vánky 1987). Some of the varying morphological traits of soral formation or spore characteristics for ustilaginomycetous families are summarized in Fig. 11.8.

Besides the majority of Ustilaginomycota, which parasitize their host in the dikaryotic phase, there are a few examples of specific haploid yeast parasites. The most prominent ones certainly belong to the genus Malassezia , in which the anamorphic lipophylic yeast species specifically feed on the skin of warm-blooded animals , where they are involved in common skin diseases (Xu et al. 2007). To date, there are more species described with different specific host substrates, i.e. the mite parasitic species of Meira and Acaromyces (Gerson et al. 2008).

III. Classification System

Beginning with Tulasne and Tulasne (1847), the smut fungi have traditionally been divided into phragmobasidiate Ustilaginaceae or Ustilaginales and holobasidiate Tilletiaceae or Tilletiales (e.g. Kreisel 1969; Oberwinkler 1987). Durán (1973) and Vánky (1987) discussed the difficulties associated with smut classification in detail but did not list higher taxa in the group. Consequently, Vánky (1987) treated all smut fungi in a single order, Ustilaginales, with one family, Ustilaginaceae. Other plant parasites like Exobasidium , Graphiola, and Microstroma are treated in other families and orders (Hennings 1900) and are included in Ustilaginomycotina on the basis of ultrastructural characters (Bauer et al. 1997).

The classification proposed below is based predominantly on characteristics of host–parasite interactions, the septal pore apparatus (Fig. 11.6) (Bauer et al. 1997), and LSU sequence analyses (Fig. 11.7) (Begerow et al. 1997, 2006). However, the system is still under discussion because many groups are still poorly studied. As mentioned previously, the position of Entorrhiza within Basidiomycota is questionable based on molecular data, and the genus lacks some typical morphological features of Ustilaginomycotina (e.g. it does not possess membranous pore caps) (Bauer et al. 1997). The phylogenetic relationships among the different families of Ustilaginales and Urocystidales could only be clarified by molecular data and revealed the convergent evolution of several characters, e.g. the loss of septal pores or the development of intracellular hyphae (Begerow et al. 2006). Although the types of basidial development are quite different among the various families of Exobasidiales or the families of Microstromatales , the relationships between the respective families within these orders are not always clear, and some of them are difficult to separate from each other without molecular data. Unresolved phylogenetic relationships are discussed with the respective groups in the next section. The fundamental characters used in classifying the Ustilaginomycotina were discussed in detail by Bauer et al. (1995a, b, 1997) and are therefore only briefly summarized here.

A. Fundamental Characters

1. Cellular Interactions

Hyphae of Ustilaginomycotina that are in contact with host plant cells possess zones of host–parasite interaction, with fungal deposits resulting from exocytosis of primary interactive vesicles . These zones provide ultrastructural characteristics diagnostic for higher groups in Ustilaginomycotina (Fig. 11.6) (Bauer et al. 1997; Begerow et al. 2006). Initially, primary interactive vesicles with electron-opaque contents accumulate in the fungal cell. Depending on the fungal species, these primary interactive vesicles may fuse with one another before exocytosis from the fungal cytoplasm. Electron-opaque deposits also appear at the host side, opposite the point of contact with the fungus (Fig. 11.4a–e). Detailed studies indicate that these deposits at the host side originate from the exocytosed fungal material by transfer towards the host plasma membrane (Bauer et al. 1995b, 1997).

The following major types, minor types, and variations were recognized by Bauer et al. (1995b, 1997, 2001a).

a.
Local interaction zones (Fig. 11.4a–d). Short- term production of primary interactive vesicles at interaction site results in local inter-action zones.
1. 1.
  Local interaction zones without interaction apparatus (Fig. 11.4a). Primary interactive vesicles fuse individually with the fungal plasma membrane. Depending on the species, local interaction zones without an interaction apparatus are present in intercellular hyphae or haustoria .
2. 2.
  Local interaction zones with interaction apparatus (Fig. 11.4b–d). Fusion of the primary interactive vesicles precedes exocytosis.
  1. a)
    Local interaction zones with simple interaction apparatus (Fig. 11.4b). Primary interactive vesicles fuse to form one large secondary interactive vesicle per interaction site. Depending on the species, interaction zones of this type are located in intercellular or intracellular hyphae.
  2. b)
    Local interaction zones with complex interaction apparatus (Fig. 11.4c, d). Numerous primary interactive vesicles fuse to form several secondary interactive vesicles per interaction site. Fusion of the secondary interactive vesicles then results in the formation of a complex cisternal net.
    1. i.
      Local interaction zones with complex interaction apparatus containing cytoplasmic compartments (Fig. 11.4c). The intercisternal space of the cisternal net finally becomes integrated in the interaction apparatus. Depending on the species, interaction zones of this type are formed by intercellular hyphae or haustoria.
    2. ii.
      Local interaction zones with complex interaction apparatus producing interaction tubes (Fig. 11.4d). The intercisternal space does not become integrated in the interaction apparatus. Transfer of fungal material to the host plasma membrane occurs in two or three steps. The first transfer results in the deposition of a tube at the host plasma membrane. Depending on the species, interaction zones of this type are located in intercellular hyphae or haustoria.
b.
Enlarged interaction zones (Fig. 11.4e). Continuous production and exocytosis of primary interactive vesicles results in the continuous deposition of fungal material at the entire contact area with the host cell. Depending on the species, this type of interaction zone is located in intercellular hyphae, intracellular hyphae, or haustoria.

2. Septation

Septal pore architecture plays an important role in the classification of the Basidiomycota (Oberwinkler 1985; Wells 1994). The pores of the Ustilaginomycotina are not associated with differentiated, multilayered caps or sacs derived from the endoplasmic reticulum. The septa produced in the saprobic phase of the dimorphic species of the Ustilaginomycotina are usually devoid of distinct septal pores. Septa in soral hyphae of the Ustilaginomycotina either have pores with membrane caps or are poreless. Five types of septation of soral hyphae were recognized by Bauer et al. (1997): (1) presence of simple pores with two tripartite membrane caps (Fig. 11.5a), (2) presence of simple pores with two outer tripartite membrane caps and two inner nonmembranous plates (Fig. 11.5b) (see also Bauer et al. 1995a), (3) presence of simple pores with two outer tripartite membrane caps and a tube in the pore channel (Fig. 11.5c), (4) presence of dolipores with membrane bands (Fig. 11.5d) (see also Roberson and Luttrell 1989), and (5) septa without distinct pores (Fig. 11.5e) designated as poroid or poreless septa.

B. Overview

In what follows, an overview of the taxa included in the Ustilaginomycotina is given. The system is based on a review of available studies. Discrepancies with other taxa proposed in the past are discussed subsequently. Compared to a previous overview (Bauer et al. 2001b), we have included several new genera, Malasseziales and Ceraceosorales, and excluded Entorrhiza, mainly based on the results of molecular analyses (Hibbett et al. 2007). Host families are indicated if the host range of the respective genera comprises one or two families. Following a unification of anamorphic and teleomorphic taxonomies (Hawksworth et al. 2011), the anamorphic species are ascribed to higher teleomorphic taxa based on molecular data (Fig 11.7) (Boekhout et al. 2011). Numbers in parentheses indicate the known species of each genus (Boekhout et al. 2011; Kirk et al. 2008; Vánky 2012; Chamnanpa et al. 2013; Denchev and Denchev 2011; Lutz et al. 2012; Savchenko et al. 2013).

Ustilaginomycotina R. Bauer, Begerow, J.P. Samp., M. Weiss & Oberw.

I.
Exobasidiomycetes: Begerow, M. Stoll, R. Bauer

a.
Ceraceosorales: : Begerow, M. Stoll & R. Bauer

i.
Ceraceosoraceae Denchev & R.T. Moore

Ceraceosorus B.K. Bakshi on Malvaceae (1)

b.
Doassansiales R. Bauer & Oberw.

i.
Melaniellaceae R. Bauer, Vánky, Begerow & Oberw.

Melaniella R. Bauer, Vánky, Begerow & Oberw. on Selaginellaceae (2)

ii.
Doassansiaceae (Azb. & Karat.) R.T. Moore emend. R. Bauer & Oberw.

Burrillia Setchell on monocots (4)

Doassansia Cornu on mono- and eudicots (12)

Doassinga Vánky, R. Bauer & Begerow on Plantaginaceae (1)

Entylomaster Vánky & R.G. Shivas on Araceae (2)

Heterodoassansia Vánky on mono- and eudicots (8)

Nannfeldtiomyces Vánky on Typhaceae (2)

Narasimhania Thirum. & Pavgi emend Vánky on Alismataceae (1)

Pseudodermatosorus Vánky on Alismataceae (2)

Pseudodoassania (Setchell) Vánky on Alismataceae (2)

Pseudotracya Vánky on Hydrocharitaceae (1)

Tracya H. & P. Sydow on Hydrocharitaceae and Araceae (2)

iii.
Rhamphosporaceae R. Bauer & Oberw.

Rhamphospora D.D. Cunn. on Nymphaeaceae (1)

c.
Entylomatales R. Bauer & Oberw.

i.
Entylomataceae R. Bauer & Oberw.

Entyloma de Bary on eudicots (163)

Tilletiopsis Derx pro parte (anamorphic) (3)

d.
Exobasidiales P. Henn. emend. R. Bauer & Oberw.

i.
Brachybasidiaceae Gäum.

Brachybasidium Gäumann on Arecaceae (1)

Dicellomyces L. S. Olive on monocots (4)

Exobasidiellum Donk on Poaceae (2)

Kordyana Racib. on Commelinaceae (5)

Meira Boekhout, Scorzetti, Gerson & Sztejnb. (anamorphic) (4)

Proliferobasidium L.J. Cunn. on Heliconiaceae (1)

ii.
Cryptobasidiaceae Malençon ex Donk

Acaromyces Boekhout, Scorzetti, Gerson & Sztejnb. (anamorphic) (2)

Botryoconis H. & P. Sydow on Lauraceae (5)

Clinoconidium Pat. on Lauraceae (2)

Coniodictyum Har. & Pat. on Rhamnaceae (1)

Drepanoconis Schröter & P. Henn. on Lauraceae (3)

Laurobasidium Jülich on Lauraceae (1)

iii.
Exobasidiaceae P. Henn.

Arcticomyces Savile on Saxifragaceae (1)

Austrobasidium Palfner on Hydrangeaceae (1)

Exobasidium Woronin on Ericales (50)

Muribasidiospora Kamat & Rajendren on Anacardiaceae and Ulmaceae (3)

iv.
Graphiolaceae E. Fischer

Graphiola Poiteau on Arecaceae (5)

Stylina H. Sydow on Arecaceae (1)

e.
Georgefischeriales R. Bauer, Begerow & Oberw.

i.
Georgefischeriaceae R. Bauer, Begerow & Oberw.

Georgefischeria Thirum. & Narash. emend. Gandhe on Convolvulaceae (4)

Jamesdicksonia Thirum., Pavgi & Payak on Cyperaceae and Poaceae (16)

ii.
Gjaerumiaceae R. Bauer, M. Lutz & Oberw.

Gjaerumia R. Bauer, M. Lutz & Oberw. on Asparagaceae , Melanthiaceae and Xanthorrhoeaceae (3)

Tilletiopsis Derx pro parte (anamorphic) (2)

iii.
Tilletiariaceae Moore

Phragmotaenium R. Bauer, Begerow, A. Nagler & Oberw. on Poaceae (1)

Tilletiaria Bandoni & Johri (1)

Tilletiopsis Derx pro parte (anamorphic) (4)

Tolyposporella Atkinson on Poaceae (6)

iv.
Eballistraceae R. Bauer, Begerow, A. Nagler & Oberw.

Eballistra R. Bauer, Begerow, A. Nagler & Oberw. on Poaceae (3)

f.
Malasseziales Moore emend. Begerow, R. Bauer & Boekhout

Malassezia Baill. (anamorphic) (14)

g.
Microstromatales R. Bauer & Oberw.

i.
Microstromataceae Jülich

Microstroma Niessl on Juglandaceae , Fabaceae and Fagaceae (4)

Rhodotorula F.C. Harrison pro parte (anamorphic) (3)

ii.
Volvocisporiaceae Begerow, R. Bauer & Oberw.

Volvocisporium Begerow, R. Bauer & Oberw. on Malvaceae (2)

iii.
Quambalariaceae Z.W. de Beer, Begerow & R. Bauer

Quambalaria J.A. Simpson on Myrtaceae (6)

Jaminaea Sipiczki & Kajdacsi (anamorphic) (2)

iv.
Microstromatales incertae sedis

Sympodiomycopsis Sugiy., Tokuoka & Komag. (anamorphic) (2)

h.
Tilletiales Kreisel ex R. Bauer & Oberw.

i.
Tilletiaceae Tul. & C. Tul. emend. R. Bauer & Oberw.

Conidiosporomyces Vánky on Poaceae (3)

Erratomyces M. Piepenbr. & R. Bauer on Fabaceae (5)

Ingoldiomyces Vánky on Poaceae (1)

Neovossia Körn. on Poaceae (1)

Oberwinkleria Vánky & R. Bauer on Poaceae (1)

Salmacisia D.R. Huff & A. Chandra on Poaceae (1)

Tilletia L. & C. Tul. on Poaceae (179)

i.
Exobasidiomycetes incertae sedis

Tilletiopsis albescens Gokhale (anamorphic)

Tilletiopsis pallescens Gokhale (anamorphic)

II.
Ustilaginomycetes R. Bauer, Oberw. & Vánky

a.
Urocystidales R. Bauer & Oberw.

i.
Doassansiopsidaceae Begerow, R. Bauer & Oberw.

Doassansiopsis (Setchell) Dietel on mono- and dicots

ii.
Floromycetaceae M. Lutz, R. Bauer & Vánky

Antherospora R. Bauer, M. Lutz, Begerow, Piątek & Vánky on Asparagaceae (8)

Floromyces Vánky, M. Lutz & R. Bauer on Asparagaceae (1)

iii.
Glomosporiaceae Cifferi emend. Begerow, R. Bauer & Oberw.

Thecaphora Fingerh. (including Glomosporium , Kochmania , Tothiella , Sorosporium ) on eudicots (61)

iv.
Mycosyringaceae R. Bauer & Oberw.

Mycosyrinx Beck on Vitaceae (4)

v.
Urocystidaceae Begerow, R. Bauer & Oberw.

Flamingomyces R. Bauer, M. Lutz, Piątek, Vánky & Oberw. on Ruppiacae (1)

Melanoxa M. Lutz, Vánky & R. Bauer on Oxalidaceae (2)

Melanustilospora Denchev on Araceae (2)

Mundkurella Thirum. on Araliaceae (5)

Urocystis Rabenh. ex Fuckel on mono- and eudicots (165)

Ustacystis Zundel on Rosaceae (1)

Vankya Ershad on Liliaceae (3)

b.
Ustilaginales Clinton emend. R. Bauer & Oberw.

i.
Anthracoideaceae Denchev

Anthracoidea Brefeld on Cyperaceae (101)

Cintractia Cornu on Cyperaceae (13)

Dermatosorus Sawada ex Ling on Cyperaceae (6)

Farysia Racib. on Cyperaceae (21)

Farysizyma A. Fonseca (anamorphic) (4)

Heterotolyposporium Vánky on Cyperaceae (1)

Leucocintractia M. Piepenbr., Begerow & Oberw. on Cyperaceae (4)

Moreaua T. N. Liou & H. C. Cheng on Cyperaceae (36)

Parvulago R. Bauer, M. Lutz, M. Piątek, Vánky & Oberw. on Cyperaceae (1)

Pilocintractia Vánky on Cyperaceae (2)

Planetella Savile on Cyperaceae (1)

Portalia V. Gonzáles, Vánky & G. Platas on Cyperaceae (1)

Schizonella Schröter on Cyperaceae (6)

Shivasia Vánky, M. Lutz & M. Piątek on Cyperaceae (1)

Stegocintractia M. Piepenbr., Begerow & Oberw. on Juncaceae (6)

Tolyposporium Woronin ex Schröter on Juncaceae (5)

Trichocintractia M. Piepenbr. on Cyperaceae (1)

Ustanciosporium Vánky emend. M. Piepenbr. on Cyperaceae (21)

ii.
Melanotaeniaceae Begerow, R. Bauer & Oberw.

Exoteliospora R. Bauer, Oberw. & Vánky on Osmundaceae (1)

Melanotaenium de Bary on eudicots (9)

Yelsemia Walker on eudicots (4)

iii.
Ustilaginaceae Tul. & C. Tul. emend. R. Bauer & Oberw.

Anomalomyces Vánky, M. Lutz & R.G. Shivas on Poaceae (1)

Anthracocystis Bref. on Poaceae (124)

Eriomoeszia Vánky on Eriocaulaceae (1)

Franzpetrakia Thirum. & Pavgi emend. Guo, Vánky & Mordue on Poaceae (3)

Langdonia McTaggart & R.G. Shivas on Poaceae (8)

Macalpinomyces Langdon & Full. emend. Vánky on Poaceae (41)

Melanopsichium G. Beck on Polygonaceae (2)

Moesziomyces Vánky on Poaceae (1)

Pericladium Pass. on Malvaceae (3)

Pseudozyma Bandoni emend. Boekhout (anamorphic) (16)

Sporisorium Ehrenb. on Poaceae (195)

Stollia McTaggart & R.G. Shivas on Poaceae (5)

Tranzscheliella Lavrov on Poaceae (17)

Triodiomyces McTaggart & R.G. Shivas on Poaceae (5)

Tubisorus Vánky & M. Lutz on Poaceae (1)

Ustilago (Pers.) Roussel on Poaceae (167)

iv.
Websdaneaceae Vánky

Restiosporium Vánky on Anarthriaceae and Restionaceae (23)

Websdanea Vánky on Anarthriaceae (1)

v.
Ustilaginales incertae sedis:

Ahmadiago Vánky on Euphorbiaceae (1)

Centrolepidosporium R.G. Shivas & Vánky on Centrolepidaceae (1)

Cintractiella K.B. Boedijn emend. M. Piepenbr. on Cyperaceae (2)

Clintamra Cordas & Durán on Asparagaceae (1)

Eriocaulago Vánky on Eriocaulaceae (2)

Eriosporium Vánky on Eriocaulaceae (2)

Farysporium Vánky on Cyperaceae (1)

Geminago Vánky & R. Bauer on Malvaceae (1)

Kuntzeomyces P. Henn. ex Sacc. & P. Sydow on Cyperaceae (2)

Orphanomyces Savile on Cyperaceae (3)

Testicularia Klotzsch on Cyperaceae (3)

Uleiella Schröter on Araucariaceae (2)

C. Description

Within Ustilaginomycotina two major groups are evident in the dendrograms resulting from ultrastructural and LSU rDNA sequence analyses (Figs. 11.6 and 11.7) (Bauer et al. 1997; Begerow et al. 2006). Though the monophyly of the Ustilaginomycetes is well supported, this is not always the case with the Exobasidiomycetes (Hibbett et al. 2007). However, in the absence of additional studies, we follow the earlier interpretations and retain Ceraceosorales and Malasseziales as part of the Exobasidiomycetes (Begerow et al. 2000, 2006). Although many morphological characters of sori and teliospores are not consistent at higher taxonomic levels, an overview at the family level is included in Fig. 11.8.

1. Exobasidiomycetes

Exobasidiomycetes represents the sister group of Ustilaginomycetes (Bauer et al. 1997; Begerow et al. 1997, 2006; Hibbett et al. 2007). The members of Exobasidiomycetes and Ustilaginomycetes share the presence of membrane caps or bands at the septal pores (Fig. 11.6). However, taxa with poreless septa evolved in both groups. Exobasidiomycetes differs from Ustilaginomycetes in the formation of local interaction zones (Fig. 11.5). Except for Tilletiariaceae (Fig. 11.3k), all members of Exobasidiomycetes are holobasidiate (Fig. 11.3f–j, l–o). Among the basidiomycetes, the formation of ballistosporic holobasidia, in which the hilar appendices of the basidiospores are oriented abaxially (sterigmata turned outwards; basidiospores inwards) (Fig. 11.3j, o), is restricted to Exobasidiomycetes . This type of basidium is common in Exobasidiales (Fig. 11.3o) but also occurs in species of Doassansiales , Georgefischeriales (Fig. 11.3j), and Tilletiales (Goates and Hoffmann 1986). Therefore, the Exobasidium basidium with the specific orientation of the ballistosporic basidiospores may represent an apomorphy for Exobasidiomycetes .

Teliospores are absent or present within the Exobasidiomycetes . Formation of teliospore balls only occurs in Doassansiaceae and in Tolyposporella . Smut fungi among the Exobasidiomycetes show terminal or intercalary teliospore formation (Roberson and Luttrell 1987; Trione et al. 1989). A gelatinization of hyphal walls preceding teliospore formation is either lacking or not clearly recognizable.

Currently we include eight orders on the basis of ultrastructural characters and molecular phylogenetic data within Exobasidiomycetes (Fig. 11.6). A superorder, Exobasidianae, including Entylomatales , Doassansiales, and Exobasidiales , was proposed based on the apomorphy of a complex interaction apparatus (Bauer et al. 1997). This grouping is highly sensitive to sampling in molecular analyses (Fig. 11.7), and therefore we follow the system of Hibbett et al. (2007). Anamorphic species without affiliation to a teleomorph have been assigned to Tilletiopsis , although the genus is non-monophyletic (Begerow et al. 2000). However, some anamorphic species or lineages have been named according to a unique ecology as in Meira and Jaminaea . The phylogenetic positions of Malasseziales and Ceraceosorales are controversial, and some authors have proposed a treatment as incertae sedis (Hibbett et al. 2007). Although apomorphic exobasidiomycetous morphological features like septal pore caps and local interaction zones are lacking, at least in Malasseziales , we follow the proposal of Begerow et al. (2006) based on molecular data (Fig. 11.7). All orders are presented alphabetically without additional hierarchy.

a) Ceraceosorales

Within Exobasidiomycetes , the Ceraceosorales are characterized by intracellular hyphae with a simple interaction apparatus (Fig. 11.6) (Begerow et al. 2006). The septal pores in Ceraceosorus bombacis (B.K. Bakshi) B.K. Bakshi are simple and enclosed by membrane caps at both sides (Fig. 11.5a), as seen in Melanotaeniaceae of the Ustilaginomycetes and in Microstromatales , Entylomatales , Doassansiales, and Exobasidiales of the Exobasidiomycetes (Bauer et al. 1997; Begerow et al. 2006). In Ceraceosorus and in Brachybasidiaceae , basidia protrude through stomata or emerge from the disintegrated epidermis. The basidia are elongated, basally thick-walled, and two-sterigmate and form ballistosporic basidiospores with an adaxial orientation of the hilar appendices in both groups (Begerow et al. 2002; Cunningham et al. 1976). Like Brachybasidiaceae and Exobasidiomycetes in general, Ceraceosorus produces local interaction zones (Begerow et al. 2006). However, molecular data do not support a closer relationship between Exobasidiales and Ceraceosorales (Fig. 11.7). The other Exobasidiomycetes lacking an interaction apparatus or establishing a simple interaction apparatus, such as Entylomatales , Georgefischeriales , Microstromatales, and Tilletiales , do not form intracellular hyphae or haustoria (Bauer et al. 1997; Begerow et al. 2006). Thus, C. bombacis (B.K. Bakshi) B.K. Bakshi seems to be isolated, and the monotypic order seems to be justified.

b) Doassansiales

A complex interaction apparatus, including cytoplasmic compartments, characterizes this order (Figs. 11.4c and 11.6) (Bauer et al. 1997). The studied species of this group have parasitic hyphae with clamps. They are teliosporic and dimorphic and do not form ballistoconidia in the haploid phase. The teliospore germinates with holobasidia (Fig. 11.3g) (Bauer et al. 1999a; Vánky et al. 1998). The members of Burrillia , Doassansia , Entylomaster , Heterodoassansia , Nannfeldtiomyces , Narasimhania , Pseudodoassansia , Pseudodermatosporus , Pseudotracya, and Tracya have complex spore balls (Vánky 1987, 2012), whereas Doassinga (Fig. 11.1a), Melaniella, and Rhamphospora produce single spores (Vánky 1994; Vánky et al. 1998). The spore balls differ in the occurrence of sterile cells within the spore ball. In addition, teliospores are darkly coloured in Melaniella and lightly coloured in Doassinga , Rhamphospora, and genera with complex teliospore balls. The hosts of the Doassansiales are systematically diverse, comprising spike mosses (Selaginellaceae ) and various monocots as well as eudicots.

However, members of Doassansiales are ecologically well characterized by their occurrence on paludal or aquatic plants, or at least on plants of moist habitats. They apparently evolved in the ecological niche of aquatic plants and developed complex spore balls and more or less sigmoid basidiospores in adaptation to water dispersal (Fig. 11.3g) (Bauer et al. 1997). Interestingly, the species of Doassansiopsis in Urocystidales likewise parasitize aquatic plants and possess similar complex spore balls. Thus, Doassansiopsis and Doassansiales are excellent examples of the independent, convergent evolution of similar structures under the same environmental condition.

The order comprises three families. Ultrastructural and LSU sequence analyses revealed a basal dichotomy between Melaniellaceae presenting pigmented spores and Rhamphosporeaceae and Doassansiaceae showing hyaline teliospores (Bauer et al. 1999a; Begerow et al. 1997). In contrast to members of Doassansiaceae , Rhamphospora nymphaeae D. Cunn., the only species placed in the Rhamphosporaceae , forms highly branched haustoria (Fig. 11.8) (Bauer et al. 1997).

c) Entylomatales

Entylomatales is characterized by the presence of a simple interaction apparatus at the interaction sites (Fig. 11.4b) and simple hyaline spores as well as simple septal pores (Fig. 11.6) (Bauer et al. 1997). This group comprises only species of Entyloma occurring on eudicots (Fig. 11.1b), with the type species of Entyloma , Entyloma microsporum (Unger) Schröter (Fig. 11.3f), as well as anamorphic Tilletiopsis species. Ultrastructural and LSU sequence analyses revealed that the genus Entyloma was polyphyletic and that the previous “Entyloma ” species occurring on monocots belonged to Georgefischeriales (designated as Eballistra or Jamesdicksonia) (Figs. 11.3i, j and 11.7) (Bauer et al. 1997; Begerow et al. 1997, 2002).

Although the species in the genus Entyloma are morphologically very similar, systematic analyses supported numerous host-specific species (Boekhout et al. 2006). The majority of Entyloma species parasitize plant families in Ranunculales or Asteridae , whereby the members of Ranunculales seem to be the older host group as its parasites are paraphyletic and show longer branch lengths (Begerow et al. 2002). Within Asteridae (including one Entyloma species on Saxifragaceae ) an “explosive” radiation seems to have occurred, most likely caused by a rapid succession of host jumps rather than co-cladogenesis (Begerow et al. 2002). This is supported by the fact that Entyloma species on closely related host groups are not necessarily closely related to each other. Additionally, the much longer branch lengths in Asteridae hosts indicate that their interaction with Entyloma is younger than the radiation of the host group (Begerow et al. 2002). Finally, the inclusion of an Entyloma species on Chrysosplenium (Saxifragaceae ) supports this view of host shifts as a likely explanation for the observed host range patterns (Begerow et al. 2002).

The anamorphic Tilletiopsis species, which have been assumed to be the sister group to Entyloma (Fig. 11.7) (Begerow et al. 2002), are now known to have evolved independently several times within the genus Entyloma (Boekhout et al. 2006). Research in this group has recently gained importance because so-called white haze, a post-harvest disorder of apples, has been associated with the proliferation of pseudomycelia of various Tilletiopsis species. This cosmetic disorder was first described as problematic under low-oxygen storage conditions but was demonstrated to additionally occur on fruits in the field. The increase in observations in the last decade is correlated mainly with an increase in humidity and new cultivation procedures in this time frame (Baric et al. 2010).

d) Exobasidiales

Members of Exobasidiales are characterized by the presence of interaction tubes produced by a complex interaction apparatus (Fig. 11.4d) (Bauer et al. 1997) and septal pores with membranous caps and an additional tube inside (Figs. 11.5c and 11.6). The monophyly of this group is also well supported by molecular data (Fig. 11.7) (Begerow et al. 2002, 2006). Members of Exobasidiales are holobasidiate and dimorphic (Fig. 11.3l–o). They do not form teliospores in the parasitic phase or ballistoconidia in the saprobic phase. In most species, the basidiospores become septate during germination. Hosts are mono- and eudicots. The sori appear on leaves, fruits, and stems (Figs. 11.1a–c and 8). We currently recognize four families in this order (Fig. 11.6) (Begerow et al. 2002; Hibbett et al. 2007).

The Brachybasidiaceae sporulate on the surface of host organs. The basidia protrude through stomata or emerge from the disintegrated epidermis. The basidia are elongated and ballistosporic and have two sterigmata. The basidiospores are thin-walled. Available data indicate that the hilar appendices of the basidiospores are oriented adaxially at the apex of the basidia (see Figs. 2, 6, 13, 17 in Cunningham et al. 1976; Fig. 1-G in Ingold 1985; Figs. 1.10-2, 1.10-3 in Oberwinkler 1982; Fig. 4 in Oberwinkler 1993). Brachybasidium pinangae Gäumann, Dicellomyces gloeosporus Olive, and Proliferobasidium heliconiae Cunningham form persistent probasidia that are arranged in delimited fructifications. The species of Brachybasidiaceae live predominantly on monocots (Cunningham et al. 1976; Gäumann 1922; Oberwinkler 1978, 1982, 1993; Olive 1945). Molecular analyses placed the anamorphic genus Meira , isolated from pear fruits, into this family, although teleomorphic stages are unknown (Rush and Aime 2013; Yasuda et al. 2006).

The non-smut family Cryptobasidiaceae (Fig. 11.1c, d) contrasts with Brachybasidiaceae and Exobasidiaceae because it sporulates internally by producing holobasidia in peripheral lacunae of the host galls (Fig. 11.6). During maturation, the galls rupture and liberate the basidiospore mass. The basidia are gastroid and lack sterigmata. The basidiospores are usually thick-walled, resembling the urediniospores of rust fungi or the teliospores of smut fungi. In addition, old fructifications often resemble smut sori. These characters may explain why some members of this group were described as smut fungi (see above), whilst others were originally described as rusts [e.g. Clinoconidium farinosum (P. Henn.) Pat. as Uredo farinosa P. Henn.]. In contrast to other members of Cryptobasidiaceae, Laurobasidium lauri (Geyler) Jülich (Fig. 11.1d) sporulates on the surface of host organs. Additionally, the basidia of this species resemble those of Exobasidium but are gastroid, as in other members of Cryptobasidiaceae [for a detailed discussion see Begerow et al. (2002)]. Thus, Laurobasidium may occupy a systematic position at the base of the Cryptobasidiaceae and intermediate between Cryptobasidiaceae and other Exobasidiales , although this is not supported by molecular analyses so far (Begerow et al. 2002). Except for Coniodictyum (Fig. 11.1c), the host range of Cryptobasidiaceae is restricted to laurels. Cryptobasidiaceae species are known only from Japan, Africa, and South America (Donk 1956; Hendrichs et al. 2003; Lendner 1920; Malençon 1953; Maublanc 1914; Oberwinkler 1978, 1982, 1993; Piepenbring et al. 2010; Sydow 1926). In molecular studies the anamorphic genus Acaromyces isolated from mites also clusters within Cryptobasidiacae (Boekhout et al. 2003).

Exobasidiaceae species are morphologically similar to those of Brachybasidiaceae . Like members of Brachybasidiaceae , Exobasidiaceae species sporulate through stomata or from the disintegrated epidermis (Mims and Richardson 2007), the basidia are elongated and ballistosporic, and the basidiospores are thin-walled. In contrast to the Brachybasidiaceae , the hilar appendices of the basidiospores are oriented abaxially at the apex of the basidia (Fig. 11.3o) (Oberwinkler 1977, 1978, 1982). In most Exobasidiaceae species, the number of sterigmata per basidium is not fixed, varying from two to eight, with four as the most frequent number. Only a few species form generally two-sterigmate basidia. Exobasidiaceae comprises Arcticomyces , Austrobasidium , Exobasidium, and Muribasidiospora (Begerow et al. 2002). The members of this family occur on eudicots predominantly on Ericaceae (Fig. 11.1e) (Hennings 1900; Mims et al. 1987; Nannfeldt 1981; Oberwinkler 1977, 1978, 1982, 1993; Piepenbring et al. 2010; Rajendren 1968).

The Graphiolaceae are parasites of palms. Fructification of the Graphiolaceae starts between chlorenchyma and hypodermal tissue (Cole 1983). During differentiation of the cupulate to cylindrical basidiocarp, the epidermis ruptures and globose basidia are produced in chains by disarticulation of sporogenous hyphae within the basidiocarps (Fig. 11.3l). The passively released basidiospores arise laterally on the basidia (Fischer 1921, 1922; Oberwinkler et al. 1982). Haustoria are constricted at the point of penetration and consist of a clamped basal body (see Fig. 11.3 in Oberwinkler et al. 1982; Bauer et al. 1997; Begerow et al. 2002).

e) Georgefischeriales

Among the Exobasidiomycetes, this group is characterized by the presence of poreless septa in soral hyphae (Fig. 11.6). The Georgefischeriales species have a dimorphic life cycle and form teliospores. They interact with their respective hosts via local interaction zones without an interaction apparatus (Bauer et al. 1997, 2001a, 2005). Haustoria or intracellular hyphae are lacking. The Georgefischeriales sporulate in vegetative parts of the hosts, predominantly in leaves (Fig. 11.1f, g). Teliospores are yellow to brown in species of Georgefischeria and darkly coloured in other taxa. The teliospore masses are usually not powdery, and host tissues are not fractured to expose the sori (Bauer et al. 1997, 2001a, 2005). The order is divided into four families, Georgefischeriaceae , Gjaerumiaceae , Tilletiariaceae, and Eballistraceae (Fig. 11.8).

Except for Georgefischeria , with its four species on Convolvulaceae and the species of Gjaerumia on several monocot families, the Georgefischeriales occur on Poales . Because Tilletiaria anomala Bandoni & B.N. Johri appeared in a plate over which a polypore growing on decaying wood had been suspended (Bandoni and Johri 1972), nothing is known of its ecology. Most recently, T. anomala was found in the intercellular spaces of rice plants, indicating an endophytic life style (Takahashi et al. 2011). In this study, other grass parasites, including Ustilago and Tilletia, were also found in the intercellular spaces, and, like T. anomala , smut fungi occasionally form teliospores and basidia in culture (Fig. 11.3k) (Bauer et al. 1997, 2005). It is conceivable that T. anomala is a phytoparasite, probably on grasses.

The molecular phylogenies of this group (Bauer et al. 2005) correlate well with the family concept proposed by Bauer et al. (2001a) (Figs. 11.6 and 11.8). Species of Georgefischeriaceae , Gjaerumiaceae, and Eballistraceae are characterized by holobasidia (Fig. 11.3i, j), whereas species of Tilletiariaceae are phragmobasidiate (Fig. 11.3k) (Bandoni and Johri 1972; Bauer et al. 2001a, 2005). The basidiospores of Georgefischeriaceae , Gjaerumiaceae, and Tilletiariaceae form Tilletiopsis -like pseudohyphal anamorphs that produce ballistoconidia (Bandoni and Johri 1972; Bauer et al. 2005). Members of Eballistraceae do not produce ballistoconidia but form budding yeasts, which are spherical to ellipsoidal in form (Singh and Pavgi 1973).

Noteworthy is the occurrence of dolipores in young septal pores of Gjaerumiaceae . So far, within the Exobasidiomycetes dolipores are only known from members of the Tilletiales . However, in contrast to members of this group, the pores of members of Gjaerumiaceae are closed during teliosporogenesis (Bauer et al. 2005).

Molecular analyses also revealed that several anamorphic species cluster within the Georgefischeriales . The current taxonomy of these species assigned to Tilletiopsis awaits revision (Boekhout et al. 2006).

f) Malasseziales

The anamorphic genus Malassezia comprises medically important, lipophylic yeasts that constitute part of the fungal microflora on the skin of warm-blooded animals (Guého et al. 1998; Findley et al. 2013). It has been placed within the Exobasidiomycetes based on molecular studies (Begerow et al. 2000, 2006). Malassezia has been found to be associated with a variety of pathological conditions in humans, including pityriasis versicolor, seborrheic dermatitis, folliculitis, and systemic infections (Gueho et al. 1998). The cell wall of Malassezia yeasts is thick and multilamellate and reveals a unique substructure with an electron-opaque, helicoidal band that corresponds to a helicoidal evagination of the plasma membrane (Guého-Kellermann et al. 2010). The sexual phase of Malassezia is unknown, although genetic analyses revealed intact mating genes (Xu et al. 2007). The position of Malassezia in the Exobasidiomycetes is surprising and suggests that Malassezia species either are phytoparasitic in the dikaryophase or originated at least from plant parasites.

g) Microstromatales

Among the Exobasidiomycetes , the Microstromatales are characterized by the presence of simple pores and local interaction zones without an interaction apparatus (Fig. 11.6) (Bauer et al. 1997). Teliospores are lacking. Hosts are often woody plants, which is similar to the ecology of Exobasidiales . Though only a few species were initially placed in this order, three families are currently recognized: Microstromataceae , Volvocisporiaceae, and Quambalariaceae (Fig. 11.8) (Begerow et al. 2001; de Beer et al. 2006).

In Microstromataceae the young basidia protrude through the stomata and sporulate on the leaf surface (Figs. 11.1h and 11.3n) (Oberwinkler 1978; Patil 1977). They are not teliosporic, and sori are mostly less than a few millimetres in diameter (Fig. 11.1h). They are characterized by single-celled, hyaline basidiospores and infect mainly trees and bushes of various eudicot families, mainly Juglandaceae, Fabaceae, and Fagaceae (Begerow et al. 2001). In culture they form budding yeasts without ballistoconidia and pseudohyphae. In contrast to most Ustilaginomycetes , the yeast cells are more or less spherical in form.

Volvocisporiaceae are characterized by large and highly septate basidiospores (Fig. 11.3m) and are known from only two species (Begerow et al. 2001; Ritschel et al. 2008). They share the ultrastructural morphology of simple septal pores and local interaction zones with all members of Microstromatales , but they are clearly separated from other families by molecular means (Ritschel et al. 2008).

In contrast to Microstromataceae and Volvocisporiaceae , members of Quambalariaceae possess septal pores with swellings resembling dolipores of other groups (Fig. 11.6) (de Beer et al. 2006). They comprise pathogens of Eucalyptus and Corymbia, and so far, almost all host taxa are native to Australia, which suggests Australia as the centre of diversity (de Beer et al. 2006; Pegg et al. 2009). Although the development of conidiophores through stomata looks very similar to basidia of Microstroma sporulations, meiosis has not been observed and the sexual state remains unclear (Pegg et al. 2009).

The known species of Microstromatales may only represent the so-called tip of the iceberg for this group. Most of them are difficult to detect in nature and could easily be overlooked. Additionally, several yeasts belonging to this group have been isolated, and their affiliation is not always clear. Beecause yeast anamorphs are common in Microstroma , addititional surveys are needed to recognize more taxa and teleomorphs. Though the included “Rhodotorula ” species seem to be anamorphic stages of Microstroma , Sympodiomycopsis spp., and Jaminaea angkorensis Sipiczki and Kajdacsi, they seem to lack close relation to any studied species (Begerow et al. 2001; Mahdi et al. 2008; Sipiczki and Kajdacsi 2009).

h) Tilletiales

The presence of dolipores in the mature septa (Fig. 11.5d) characterizes the Tilletiales among the Exobasidiomycetes (Fig. 11.6) (Bauer et al. 1997). In contrast to all other groups of the Exobasidiomycetes , the Tilletiales are not known to be dimorphic. They form local interaction zones without an interaction apparatus (Fig. 11.4a), and their hyphal anamorphs regularly produce ballistoconidia (e. g., Carris et al. 2006; Ingold 1987b, 1997). Among all the smut fungi studied in culture, only the members of Tilletiales present distinct pores in the septa of saprobic hyphae.

Members of Tilletiales lack haustoria and intracellular hyphae (Fig. 11.8). The teliospores are darkly pigmented and often ornamented. Moreover, these teliospores are usually much larger than those of other groups of the Ustilaginomycotina, and they are never arranged in balls (Fig. 11.8). The teliospores of some species produce trimethylamine, which causes a foul smell in the spores. Seven genera are described in this family, six of which exclusively parasitize Poaceae . The genus Erratomyces is solely parasitic on Fabaceae . Sori are formed in ovaries of the hosts in the majority of species (Fig. 11.1i); only a few species of Tilletia and Erratomyces form teliospores in vegetative host organs (Castlebury et al. 2005; Piepenbring and Bauer 1997; Vánky 1994, 2012; Vánky and Bauer 1992, 1995, 1996). The teliospores germinate with holobasidia, producing terminal basidiospores, which often conjugate and give rise to infectious hyphae (Ingold 1989b; Vánky 2012).

Some species of Tilletia are economically important. Tilletia caries (DC) Tul. & C. Tul. and T. controversa J.G. Kühn on wheat and Tilletia horrida Takah. on rice can cause heavy losses in grain production (Carris et al. 2006; Mathre 1996; Trione 1982). In India and the American tropics the angular black spot disease on leaves of beans is caused by Erratomyces patelii (Pavgi & Thirum.) M. Piepenbr. & Bauer (Piepenbring and Bauer 1997).

Within Tilletiales the taxonomy is far from resolved. Molecular data especially provided controversial results for morphology-based classification (Castlebury et al. 2005). Species concepts and species delimitations are still in discussion (Cai et al. 2011). Additionally, the discovery and addition of new species might change the taxonomic concept (Bao et al. 2010; Shivas 2009).

Remarkably, Salmacisia buchloëana (Kellerm. & Swingle) D.R. Huff & Amb. Chandra parasitizing the buffalograss Buchloë dactyloides (Nutt.) Englem induces the development of ovaries in male flowers, which leads to hermaphroditism and castration of its host plant (Chandra and Huff 2008). Alteration of host reproductive structures evolved at least three times independently within smut fungi, as seen in Salmacisia , Microbotryum spp. and Thecaphora oxalidis (Ellis & Tracy) M. Lutz, R. Bauer & Piątek (Roets et al. 2008; Schäfer et al. 2010).

2. Ustilaginomycetes

The presence of enlarged interaction zones (Fig. 11.4e) characterizes this group (Fig. 11.6) (Bauer et al. 1997). The members of the Ustilaginomycetes are teliosporic, gastroid, and dimorphic. The species isolated in the anamorphic phase are usually placed in the genus Pseudozyma . However, for some members closely related to Farysia a new genus, Farysizyma, has been proposed (Inácio et al. 2008). Based on the new regulations of dual nomenclature, they should be included in Farysia (Hawksworth 2011; Hawksworth et al. 2011)

Morphologically and ecologically, members of the Ustilaginomycetes are diverse (Fig. 11.1j–p) (Vánky 1987, 1994, 2012), but both ultrastructural and LSU sequence analyses unite them (Figs. 11.6 and 11.7) (Bauer et al. 1997; Begerow et al. 1997, 2006). Two orders are recognized.

a) Urocystidales

As part of Ustilaginomycetes the Urocystidales were originally characterized by the presence of haustoria and pores in the septa of soral hyphae (Bauer et al. 1997). The morphological characterization has discrepancies with molecular data, the latter supporting the inclusion of five families: Doassansiopsidaceae , Floromycetaceae , Glomosporiaceae , Mycosyringaceae, and Urocystidaceae (Fig. 11.6) (Begerow et al. 2006; Vánky et al. 2008b). Doassansiopsidaceae , Floromycetaceae, and Urocystidaceae are characterized by the presence of haustoria and pores in the septa of soral hyphae (Bauer et al. 1997), but these characters are missing in the mature infection stuctures of Mycosyringacea e and Glomosporiaceae (Begerow et al. 2006; Vánky 1996). Additionally, molecular studies do not support the monophyly of Urocystidaceae , Doassansiopsidaceae, or Melanotaeniaeae , which are characterized by the same combination of haustoria and septal pores (Fig. 11.6). Therefore, Melanotaeniaceae is no longer part of the Urocystidales but is in the Ustilaginales (Begerow et al. 2006).

Doassansiopsidaceae shares with Urocystidaceae and Floromycetaceae an essentially identical septal pore apparatus (Fig. 11.5b) (Bauer et al. 1997). It is composed of a simple pore with two outer tripartite membrane caps and two inner non-membranous plates (Fig. 11.5b) (Bauer et al. 1995a, 1997, 2008; Vánky et al. 2008b). The species of Doassansiopsis , the only genus of Doassansiopsidaceae , possess complex teliospore balls. A central mass of pseudoparenchymatous cells is surrounded by a layer of firmly adhering, lightly coloured teliospores and an external cortex of sterile cells (Piątek et al. 2008; Vánky 1987). Doassansiopsis species form gastroid holobasidia and yeast anamorphs without ballistoconidia. The position of Doassansiopsis in Urocystidales is surprising. Based on teliospore ball morphology and the parasitism of aquatic plants, Doassansiopsis was grouped with Burillia , Doassansia , Heterodoassansia , Nannfeldtiomyces , Narasimhania , Pseudodoassansia, and Tracya (Vánky 1987, 1994). However, both ultrastructural and molecular analyses show that Doassansiopsis is not closely related to the other complex teliospore-ball-forming taxa (Fig. 11.8) (Bauer et al. 1997; Begerow et al. 1997, 2006).

Floromycetaceae includes species that parasitize various members of Asparagaceae . Within this family, haustoria and septal pores in soral hyphae are present. The genus Antherospora forms single spores in the anthers of the host plant (Bauer et al. 2008), whereas Floromyces forms spore balls in flowers. The germination of the teliospores of both genera results in phragmobasidia with sterigmata (Vánky et al. 2008b).

The family Glomosporiaceae experienced a reclassification on the basis of molecular data (Begerow et al. 2006). Originally it was included in the Ustilaginales because intracellular hyphae are formed in the host interaction (Bauer et al. 1997). Glomosporium and Tothiella were identified as synonyms of Thecaphora (Vánky et al. 2007, 2008a). Thecaphora species parasitize eudicots and display light brown teliospore balls that differ in the amount of spores (Fig. 11.1j). In the majority of species, these spore balls only consist of fertile cells, in contrast to other families within Urocystidales (Fig. 11.8). The balls vary in their integrity; in some species the balls are strongly agglutinated, whilst in other species they separate easily. Moreover, there are species that have single spores, for example T. thlaspeos (Beck) Vánky (Vánky et al. 2007, 2008a). Teliospore germination among species of Thecaphora is variable, ranging from true holobasidia to aseptate or septate hyphae that sometimes bear basidiospores (Ingold 1987c; Kochman 1939; Nagler 1986; Piepenbring and Bauer 1995). We interpret these hyphal germinations as atypical germinations resulting possibly from non-optimal environmental conditions. For example, both germination types (i.e. phragmo- and holobasidia) have been reported for Thecaphora haumanii Speg. (Piepenbring and Bauer 1995).

Mycosyringaceae is represented by a single genus, Mycosyrinx . Its host range is restricted to members of Vitaceae (Vánky 1996, 2012). The teliospores come in pairs. Germination, only known from M. cissi (DC.) G. Beck, results directly in basidiospores with a sigmoid shape (Fig. 11.3e) (Piepenbring and Bauer 1995; Vánky 1996). The basidia seem to be small or reduced, and the meiosporangium is represented by the teliospore. The fungus does not form haustoria or intracellular hyphae in host cells (Bauer et al. 1997). At maturity, soral hyphae lack septal pores (Fig. 11.5e) (Begerow et al. 2006).

Urocystidaceae comprises morphologically diverse species with coloured teliospores in flowers or leaves and stems (Fig. 11.1k, l). The genera Flamingomyces , Melanustilospora, and Vankya have single teliospores. The separation of the genera is based on the results of morphological or molecular data (Bauer et al. 2007; Denchev 2003; Ershad 2000). The genus Melanoxa also has single teliospores, but the wall of the teliospores is multilamellate (Lutz et al. 2011). Mundkurella is characterized by one- to four-celled teliospores, and Urocystis and Ustacystis by teliospores that are united in balls with fertile and sterile cells (Vánky 1987, 1994, 2012). The teliospore germination within Urocystidaceae is also diverse. Flamingomyces germinates with a single hypha; Mundkurella , Ustacystis, and Vankya (Vánky 2012; Zundel 1945) germinate with phragmobasidia, whereas Urocystis germinates with holobasidia (Fig. 11.3d) (Ingold 1999). The members of Urocystidaceae form a yeast-like anamorph without ballistoconidia.

With the advent of molecular systematics, the evolutionary trends in Urocystidales became less obvious. Urocystidales includes sporeball-forming as well as single-spore-bearing taxa, and neither sporeball formation nor basidial morphology provides a clear distinction between the different lineages as in the Georgefischeriales or Exobasidiales (Bauer et al. 2001a; Begerow et al. 2002). Given the size and diversity of the group, further studies are needed to understand the ecology and evolution that resulted in morphological variation during the radiations within Urocystidales .

b) Ustilaginales

Poreless septa characterize the Ustilaginales in general (Figs. 11.5e and 11.6). Most of the species sporulate in the reproductive parts of their hosts (Fig. 11.1m–p), and teliosporogenesis occurs by disarticulation. A prominent gelatinization of hyphal walls usually precedes teliospore formation (Luttrell 1987; Mims and Snetselaar 1991; Mims et al. 1992; Snetselaar and Mims 1994; Snetselaar and Tiffany 1990). They have darkly coloured teliospores and usually germinate with four-celled phragmobasidia (Fig. 11.3a–c). Depending on the species and sometimes on the environmental conditions, phragmobasidia vary in morphology (Ingold 1983, 1987a, 1989a, 1989c). Previously, a basal dichotomy in Ustilaginales was accepted at the family level, i.e. Glomosporiaceae and Ustilaginaceae . The system according to Bauer et al. (1997) was based on morphological and anatomical apomorphies and suggested a subdivision into Glomosporiaceae , Mycosyringaceae, and Ustilaginaceae (including Anthracoideaceae and Websdaneaceae ) (Bauer et al. 1997). However, this grouping was incongruent with molecular phylogenies favouring a dichotomy between Melanotaeniaceae and Ustilaginaceae in the Ustilaginales and Glomosporiaceae and Mycosyringaceae as part of the Urocystidales (Begerow et al. 1997). The split of Ustilaginaceae s.l. on Poales in favour of three families on different plant families suggests a host specificity of monophyletic lineages, which is not supported by most phylogenetic analyses (Begerow et al. 1997, 2000; Stoll et al. 2005). Thus, the systematics of Ustilaginales is far from settled, and our grouping reflects ongoing discussion. Based on a combination of morphology, host specificity, and LSU sequence analyses the Ustilaginales are grouped into four families (Figs. 11.6 and 11.7) (Begerow et al. 2006). Several additional, mostly monotypic, families have been proposed based on either morphological specialities or host range (Denchev 1997; Vánky 2000, 2001, 2003). For some species like Melanopsichium or Dermatosorus it can be shown that the proposed apomorphies do not provide additional systematic information (cf. Fig. 11.8), and therefore we follow the concept proposed by Begerow et al. (2006). The families of the Ustilaginales are characterized by host specificity on the family level or higher, i.e. eudicots for the Melanotaeniaceae , Anathriaceae and Restionaceae for the Websdaneaceae , Cyperaceae and Juncaceae for the Anthracoideaceae, and Poaceae for the Ustilaginaceae , thereby ignoring the fact that host jumps to distantly related hosts occurred several times, e.g. Melanopsichium or Pericladium . Vánky (2011) argued on the basis of a germination that resembles holobasidia and the isolated molecular position of Pericladium to establish a new family, Pericladiaceae . However, as long as a comprehensive molecular analysis presenting clear family concepts for the whole order is still lacking, we treat several genera in a preliminary state as incertae sedis. At the present state of knowledge, we propose the following families (Fig. 11.6).

The first family, which was excluded from Ustilaginaceae sensu Bauer et al. 1997, was Anthracoideaceae (Denchev 1997). Species of Anthracoidea present a unique type of two-celled basidia (Fig. 11.3c) and almost exclusively parasitize species of Carex . They exhibit an expanding element in their LSU sequence, which complicates their alignment with other smut species (Hendrichs et al. 2005). In molecular analyses there is no clear separation between Anthracoidea species and Cintractia -like smuts (Figs. 11.1n and 11.3b). Therefore, one family of smuts on Juncaceae and Cyperaceae was proposed (Begerow et al. 2006). In addition to the common host group, they are morphologically and ecologically similar, often presenting a whitish peridium in immature sori, which are produced in flowers or inflorescences (Fig. 11.8). Based on molecular data, members of Anthracoidea , Cintractia , Dermatosorus , Farysia , Farysizyma , Heterotolyposporium , Leucocintractia , Moreaua , Parvulago , Pilocintractia , Planetlla , Portalia , Schizonella , Stegocintractia , Tolyposporium , Trichocintractia, and Ustanciosporium are included (Begerow et al. 2006). Consequently, Cintractiaceae , Dermatosoraceae, and Farysiaceae (Vánky 2001) are rejected because they are interspersed in Anthracoideaceae .

Melanotaeniaceae is represented by Melanotaenium on eudicots (Fig. 11.1o) and Exoteliospora on Osmunda. Previous members on Poacecae have been excluded based on morphological and molecular data and are now part of the Georgefischeriales (Begerow et al. 2001). In contrast to the other three families, members of Melanotaeniaceae are characterized by simple septal pores with membrane caps and by the development of haustoria (Fig. 11.6) (Bauer et al. 1997; Begerow et al. 2006).

Ustilaginaceae comprises the large genera Ustilago and Sporisorium and several smaller genera of species previously treated as Ustilago or Sporisorium, representing a large Ustilago–Sporisorium–Macalpinomyces complex with more than 550 species. Except for Eriomoeszia , Melanopsichium, and Pericladium, all species parasitize Poaceae . Melanopsichium pennsylvanicum Hirschh., which occurs on Polygonaceae , is well embedded in the supported group of the Ustilaginaceae (Fig. 11.7). This indicates that jumps to distantly related hosts occasionally occur. However, no further radiations on Polygonaceae took place, which supports the important adaptation of the Ustilaginaceae to hosts of Poaceae . Several molecular studies have shown that the separation of Ustilago and Sporisorium is very difficult on the basis of hitherto used features (Stoll et al. 2003, 2005). Some genera have been proposed to accommodate species with clear apomorphies like Eriomoeszia , Anomalomyces , Portalia, or Tubisorus (Gonzales et al. 2007; Vánky 2005; Vánky and Lutz 2011; Vánky et al. 2006), but a clear structure of the group was lacking. Most recently, a four-gene phylogeny, combined with detailed studies on sorus morphology, revealed some monophyletic groups that could be excluded from the large Ustilago–Sporisorium–Macalpinomyces complex (McTaggart et al. 2012a, b). Based on these data, Anthracocystis was reestablished and Langdonia , Stollia, and Triodiomyces were newly described to accommodate the well-characterized monophyletic groups, together with Ustilago and Sporisorium (McTaggart et al. 2012c). Besides the host specificity of some groups, the genera are based mainly on characteristics of teliospores and sori, e.g. teliospores free or united in balls and the presence or absence of peridia, columellae, sterile cells, or sterile hyphae (see Vánky 1987, 1994). The sori of Sporisorium species are also covered by peridia, but these can be composed of host tissue or fungal hyphae. The teliospores are free or arranged in balls. Teliospore balls and special soral structures are lacking in Ustilago species, whose simple teliospores develop by replacing host organs, at least partially.

Websdaneaceae includes Websdanea and Restiosporium , both of which occur on Anarthriaceae and Restionaceae . This group is well supported in several molecular phylogenetic analyses (Begerow et al. 2006). Morphologically, they are very similar to members of Anthracoideaceae , but LSU sequence data support a sister group relationship with the other members of Ustilaginales on grasses and grass-like hosts (Fig. 11.7).

Based mainly on host relationships, Vánky (2001) created the Clintamraceae for Clintamra , Geminaginaceae for Geminago and Uleiellaceae for Uleiella . Unfortunately, molecular data are not available for these genera, and it is unclear whether these genera represent recent or ancient host jumps. Because there is no other support for these families at the moment, we treat them as incertae sedis, together with other genera lacking molecular data and clear morphological characteristics to place them in one of the described groups.

IV. Conclusions

The history of smut systematics dates back to the brothers Tulasne, who separated holobasidiate and phragmobasidiate groups for the first time (Tulasne and Tulasne 1847). This grouping was consistent for more than 100 years and to our knowledge was never questioned. Differences in the sugar composition of the cell wall of Ustilago and Microbotryum yeasts implicated a separation of smuts on monocots and dicots (Prillinger et al. 1993), but subsequent data did not support this hypothesis. The discovery of ultrastructural markers in the host–parasite interaction and septal formation provided apomorphic characters to delimit monophyletic groups which were supported by molecular analyses (Figs. 11.6 and 11.7) (Bauer et al. 1997; Begerow et al. 1997, 2006). Thus, the analysis of two characters remains to be discussed: basidia and host specificity. Their analyses reveal novel conclusions about the evolution of Ustilaginomycotina .

A. Basidia

The evolutionary transitions to the basidium of the Ustilaginomycotina are unknown. Nevertheless, a tentative sequence can be outlined from the distribution of the basidial types among the different groups. While the Agaricomycotina are dominated by the presence of holobasidia, and the Pucciniomycotina have almost exclusively phragmobasidia, the Ustilaginomycotina are somewhat intermediate, having both types in several groups (Fig. 11.3). The monophyly of the Agaricomycotina with the Ustilaginomycotina and the group’s common ancestor with the Pucciniomycotina suggest that the plesiomorphic state of the basidium was phragmobasidiate. In the Ustilaginomycetes and Exobasidiomycetes , however, phragmobasidia occur only in the Anthracoideaceae , Urocystidaceae , Ustilaginaceae , Tilletiariaceae, and Websdaneaceae . Except for a few species, the phragmobasidial taxa of the Ustilaginomycetes and Exobasidiomycetes are concentrated in a single monophyletic group of the Ustilaginales , whereas the holobasidial taxa are distributed throughout all orders of the Ustilaginomycetes and Exobasidiomycetes . In addition, the early-diverged lineages of the Ustilaginomycetes and Exobasidiomycetes , i.e. Melanotaeniaceae , Glomosporiaceae , Tilletiales, and Exobasidiales , are holobasidiate. This distribution of basidial types supports a holobasidiate ancestor of the Ustilaginomycetes and Exobasidiomycetes . Consequently, the septation of the basidia in several families must be interpreted as the result of convergent evolution. Apart from septation, the hilar appendices responsible for the active discharge of basidiospores are unevenly distributed. Though they are present in several families of the Exobasidiomycetes showing various orientations, they seem to be absent in the Ustilaginomycetes . Hence, the gastroid basidia of Ustilaginomycetes might represent an apomorphy of this monophyletic group.

B. Host Specificity

Following the reorganization of the Ustilaginomycotina systematics on the basis of phylogenetic data, it became evident that most species were highly host-specific. Moreover, monophyletic lineages are often restricted to monophyletic host groups (Begerow et al. 2004). As partly discussed earlier, within the Ustilaginomycotina there are evident examples of co- evolution with angiosperm lineages (e.g. Tilletiales , Georgefischeriales, and the Ustilago -Sporisorium complex with Poaceae , Graphiola with palms , Anthracoidea with Cyperaceae , Mycosyrinx with Vitaceae , Exobasidium with Ericales ). On the other hand, Doassansiales and Doassansiopsis are two excellent examples of evolution within a given ecosystem.

As a whole, the host range of Ustilaginomycotina is restricted to angiosperms, with a few exceptions on gymnosperms and ferns, which are regarded as the result of host jumps (Bauer et al. 1997; Begerow et al. 2004). Most Ustilaginomycotina members are parasites of monocots, especially members of Poaceae and Cyperaceae . This host distribution suggests that the Ustilaginomycotina species may have evolved as pathogens, either on early angiosperms or on early monocots, with subsequent jumps to eudicots. Given the relative age of the stem group of Ustilaginomycotina of at least 300 million years (Taylor and Berbee 2006), it seems most likely that ancestral lineages date back before the radiation of angiosperms. Thus, the present specificity of some lineages could be the result of massive extinctions during evolution. In contrast, broad host ranges of some groups, e.g. the Georgefischeriales on Poaceae with a few species on Convolvulaceae and Cyperaceae , the Tilletiales on Poaceae with five species on Leguminosae , and the Ustilaginaceae on monocots with a few genera on eudicots, indicate not only that the ancestors of Ustilaginomycotina have undergone periods of parallel evolution with their hosts, but host jumps may have stimulated the evolution of a large number of taxa.

Thus, host specificity seen in genera like Ustilago and Tilletia on Poaceae (Stoll et al. 2005) or Entyloma on asterids (Begerow et al. 2002) might be a result of adaptive radiation. Branch lengths of molecular analyses suggest radiations in these genera, which are younger than some 100–200 million years old.

C. Evolutionary Trends

Finally, our analyses suggest the following evolutionary trends within Ustilaginomycotina :

Cellular interactions from simple to complex forms;
Multiple convergent evolution of intracellular fungal elements;
Multiple convergent evolution of spore balls;
Repeated loss of septal pores in senescent hyphae;
Repeated loss of teliospores as propagules;
Multiple convergent evolution of gastroid taxa;
Repeated loss of ballistosporic mechanism;
Repeated change of sorus location from vegetative organs to flowers;
Multiple convergent evolution of sporulation in anthers;
Coevolution with host groups, but also with ecosystems;
Repeated jumps to unrelated hosts.

References

Abdel-Motaal FF, El-Zayat SA, Kosaka Y, El-Sayed MA, Nassar MSM, Ito S (2009) Four novel ustilaginomycetous anamorphic yeast species isolated as endophytes from the medicinal plant Hyoscyamus muticus. Asian J Plant Sci 8:526–535
Google Scholar
Aime MC, Toome M, McLaughlin DJ (2014) Pucciniomycotina. In: McLaughlin DJ, Spatafora JW (eds) Systematics and evolution. Springer, Heidelberg
Google Scholar
Bandoni RJ, Johri BN (1972) Tilletiaria: a new genus in the Ustilaginales. Can J Bot 50:39–43
Google Scholar
Bao X, Carris LM, Huang G (2010) Tilletia puccinelliae, a new species of reticulate-spored bunt fungus infecting Puccinellia distans. Mycologia 120:613–623. doi:10.3852/09-135
Google Scholar
Baric S, Lindner L, Marschall K, Dalla Via J (2010) Haplotype diversity of Tilletiopsis spp. causing white haze in apple orchards in Northern Italy. Plant Pathol 59:535–541. doi:10.1111/j.1365-3059.2009.02217.x
CAS Google Scholar
Bauer R, Mendgen K, Oberwinkler F (1995a) Septal pore apparatus of the smut Ustacystis waldsteiniae. Mycologia 87:18–24
Google Scholar
Bauer R, Mendgen K, Oberwinkler F (1995b) Cellular interaction of the smut fungus Ustacystis waldsteiniae. Can J Bot 73:867–883
Google Scholar
Bauer R, Oberwinkler F, Vánky K (1997) Ultrastructural markers and systematics in smut fungi and allied taxa. Can J Bot 75:1273–1314
Google Scholar
Bauer R, Oberwinkler F, Vánky K (1999a) Ustilaginomycetes on Osmunda. Mycologia 91:669–675
Google Scholar
Bauer R, Vánky K, Begerow D, Oberwinkler F (1999b) Ustilaginomycetes on Selaginella. Mycologia 91:475–484
Google Scholar
Bauer R, Begerow D, Nagler A, Oberwinkler F (2001a) The Georgefischeriales: a phylogenetic hypothesis. Mycol Res 105:416–424
Google Scholar
Bauer R, Begerow D, Oberwinkler F, Piepenbring M, Berbee ML (2001b) Ustilaginomycetes. In: McLaughlin DJ, McLaughlin EG, Lemke PA (eds) The Mycota, vol 7B, Systematics and evolution. Springer, Berlin, pp 57–83
Google Scholar
Bauer R, Lutz M, Oberwinkler F (2005) Gjaerumia, a new genus in the Georgefischeriales (Ustilaginomycetes). Mycol Res 109:1250–1258
CAS PubMed Google Scholar
Bauer R, Begerow D, Sampaio JP, Weiss M, Oberwinkler F (2006) The simple-septate basidiomycetes: a synopsis. Mycol Prog 5:41–66
Google Scholar
Bauer R, Lutz M, Piątek M, Vánky K, Oberwinkler F (2007) Flamingomyces and Parvulago, new genera of marine smut fungi (Ustilaginomycotina). Mycol Res 111:1199–1206
CAS PubMed Google Scholar
Bauer R, Lutz M, Begerow D, Piątek M, Vánky K, Bacigálová K, Oberwinkler F (2008) Anther smut fungi on monocots. Mycol Res 112:1297–1306
PubMed Google Scholar
Begerow D, Bauer R, Oberwinkler F (1997) Phylogenetic studies on nuclear large subunit ribosomal DNA sequences of smut fungi and related taxa. Can J Bot 75:2045–2056
CAS Google Scholar
Begerow D, Bauer R, Boekhout T (2000) Phylogenetic placements of ustilaginomycetous anamorphs as deduced from nuclear LSU rDNA sequences. Mycol Res 104:53–60
CAS Google Scholar
Begerow D, Bauer R, Oberwinkler F (2001) Muribasidiospora: Microstromatales or Exobasidiales? Mycol Res 105:798–810
Google Scholar
Begerow D, Bauer R, Oberwinkler F (2002) The Exobasidiales: an evolutionary hypothesis. Mycol Prog 1:187–199
Google Scholar
Begerow D, Göker M, Lutz M, Stoll M (2004) On the evolution of smut fungi on their hosts. In: Agerer R, Piepenbring M, Blanz P (eds) Frontiers in basidiomycote mycology. IHW, Echingen, German, pp 81–98
Google Scholar
Begerow D, Stoll M, Bauer R (2006) A phylogenetic hypothesis of Ustilaginomycotina based on multiple gene analyses and morphological data. Mycologia 98:906–916
PubMed Google Scholar
Bellés JM, Garro R, Pallás V, Fayos J, Rodrigo I, Conejero V (2006) Accumulation of gentisic acid as associated with systemic infections but not with the hypersensitive response in plant-pathogen interactions. Planta 223:500–511
PubMed Google Scholar
Boekhout T (2011) Tilletiopsis Derx ex Derx (1930). In: Kurtzman CP, Fell JW, Boekhout T (eds) The yeasts: a taxonomic study, 5th edn. Elsevier, London, pp 2003–2014
Google Scholar
Boekhout T, Theelen B, Houbraken J, Robert V, Scorzetti G, Gafni A, Gerson U, Sztejnberg A (2003) Novel anamorphic mite-associated fungi belonging to the Ustilaginomycetes: Meira geulakonigii gen. nov., sp. nov., Meira argovae sp. nov. and Acaromyces ingoldii gen. nov., sp. nov. Int J Syst Evol Microbiol 53:1655–1664
CAS PubMed Google Scholar
Boekhout T, Gildemacher P, Theelen B, Müller WH, Heijne B, Lutz M (2006) Extensive colonization of apples by smut anamorphs causes a new postharvest disorder. FEMS Yeast Res 6:63–76
CAS PubMed Google Scholar
Boekhout T, Guého E, Mayser P, Velegraki A (2010) Malassezia and the skin. Science and clinical practice. Springer, Berlin
Google Scholar
Boekhout T, Fonseca A, Sampaio JP, Bandoni RJ, Kwon-Chung KJ (2011) Discussion of teleomorphic and anamorphic basidiomycetous yeasts. In: Kurtzman CP, Fell JW, Boekhout T (eds) The yeasts: a taxonomic study, 5th edn. Elsevier, London, pp 1339–1372
Google Scholar
Branda E, Turchetti B, Diolaiuti G, Pecci M, Smiraglia C, Buzzini P (2010) Yeast and yeast-like diversity in the southernmost glacier of Europe (Calderone Glacier, Apennines, Italy). FEMS Microbiol Ecol 72:354–369
CAS PubMed Google Scholar
Brefeld O (1883) Botanische Untersuchungen über Hefepilze. 5. Die Brandpilze I (Ustilagineen). A. Felix, Leipzig, Germany
Google Scholar
Brefort T, Doehlemann G, Mendoza-Mendoza A, Reissmann S, Djamei A, Kahmann R (2009) Ustilago maydis as a pathogen. Annu Rev Phytopathol 47:423–445
CAS PubMed Google Scholar
Butin H, Peredo HL (1986) Hongos parásitos en coníferas de América del Sur, con especial referencia a Chile. Biblioth Mycol 101:1–100
Google Scholar
Cai L, Giraud T, Zhang N, Begerow D, Cai G, Shivas RG (2011) The evolution of species concepts and species recognition criteria in plant pathogenic fungi. Fungal Divers 50:121–133
Google Scholar
Carris LM, Castlebury LA, Goates BJ (2006) Nonsystemic bunt fungi-Tilletia indica and T. horrida: a review of history, systematics, and biology. Annu Rev Phytopathol 44:113–133
CAS PubMed Google Scholar
Castlebury LA, Carris LM, Vánky K (2005) Phylogenetic analysis of Tilletia and allied genera in order Tilletiales (Ustilaginomycetes; Exobasidiomycetidae) based on large subunit nuclear rDNA sequences. Mycologia 97:888–900
CAS PubMed Google Scholar
Chamnanpa T, Limtong P, Srisuk N, Limtong S (2013) Pseudozyma vetiver sp. nov., a novel anamorphic ustilaginomycetous yeast species isolated from the phylloplane in Thailand. Antonie Von Leeuwenhoek 104(5):637–44
Google Scholar
Chandra A, Huff DR (2008) Salmacisia, a new genus of Tilletiales: reclassification of Tilletia buchloeana causing induced hermaphroditism in buffalograss. Mycologia 100:81–93
CAS PubMed Google Scholar
Christensen JJ (1963) Corn smut caused by Ustilago maydis. Am Phytopathol Soc Monogr 2, 41 pp
Google Scholar
Cole GT (1983) Graphiola phoenicis: a taxonomic enigma. Mycologia 75:93–116
Google Scholar
Connell L, Redman R, Craig S, Scorzetti G, Iszard M, Rodriguez R (2008) Diversity of soil yeasts isolated from South Victoria Land, Antarctica. Microb Ecol 56:448–459
CAS PubMed Google Scholar
Cunningham JL, Bakshi BK, Lentz PL (1976) Two new genera of leaf-parasitic fungi (Basidiomycetidae: Brachybasidiaceae). Mycologia 68:640–654
Google Scholar
De Bary A (1884) Vergleichende Morphologie und Biologie der Pilze, Mycetozoen und Bacterien. Verlag W. Engelmann, Leipzig, Germany
Google Scholar
De Beer ZW, Begerow D, Bauer R, Pegg GS, Crous PW, Wingfield MJ (2006) Phylogeny of the Quambalariaceae fam nov., including important eucalyptus pathogens in South Africa and Australia. Stud Mycol 55:289–298
PubMed Central PubMed Google Scholar
De Vienne DM, Refrégier G, Hood ME, Guigue A, Devier B, Vercken E, Smadja C, Deseille A, Giraud T (2009) Hybrid sterility and inviability in the parasitic fungal species complex Microbotryum. J Evol Biol 22:683–698
PubMed Google Scholar
Denchev CM (1997) Anthracoideaceae, a new family in the Ustilaginales. Mycotaxon 64:411–417
Google Scholar
Denchev CM (2003) Melanustilospora, a new genus in the Urocystales (smut fungi). Mycotaxon 87:475–477
Google Scholar
Denchev CM, Denchev TT (2011) Anthracoidea melanostachyae sp. nov. (Anthracoideaceae). Mycol Balc 8:153–155
Google Scholar
Djamei A, Schipper K, Rabe F, Ghosh A, Vincon V, Kahnt J, Osorio S, Tohge T, Fernie AR, Feussner I, Feussner K, Meinicke P, Stierhof YD, Schwarz H, Macek B, Mann M, Kahmann R (2011) Metabolic priming by a secreted fungal effector. Nature 478:395. doi:10.1038/nature10454
CAS PubMed Google Scholar
Doehlemann G, van der Linde K, Aßmann D, Schwammbach D, Hof A, Mohanty A, Jackson D, Kahmann R (2009) Pep1, a secreted effector protein of Ustilago maydis, is required for successful invasion of plant cells. PLoS Pathog 5(2):e1000290. doi:10.1371/journal.ppat.1000290
PubMed Central PubMed Google Scholar
Donk MA (1956) The generic names proposed for hymenomycetes-VI. Brachybasidiaceae, Cryptobasidiaceae, Exobasidiaceae. Reinwardtia 4:113–118
Google Scholar
Durán R (1973) Ustilaginales. In: Ainsworth GC, Sparrow FK, Sussman AS (eds) The fungi, vol 4B. Academic, New York, pp 281–300
Google Scholar
Ershad D (2000) Vankya, a new genus of smut fungi. Rostaniha 1:65–72
Google Scholar
Fell JW, Statzell-Tallman A, Scorzetti G, Gutiérrez MH (2011) Five new species of yeasts from fresh water and marine habitats in the Florida Everglades. Antonie Van Leeuwenhoek 99:533–549
PubMed Google Scholar
Filonow AB (2001) Butyl acetate and yeasts interact in adhesion and germination of Botrytis cinerea conidia in vitro and in fungal decay of golden delicious apple. J Chem Ecol 27:831–844
CAS PubMed Google Scholar
Findley K, Oh J, Yang J, Conlan S, Deming C, Meyer JA, Schoenfeld D, Nomicos E, Park M, NIH Intramural Sequencing Center Comparative Sequencing Program, Kong HH, Segre JA (2013) Topographic diversity of fungal and bacterial communities in human skin. Nature 498:367–370
CAS PubMed Central PubMed Google Scholar
Fischer E (1921) Zur Kenntnis von Graphiola and Farysia. Ann Mycol 18:118–197
Google Scholar
Fischer E (1922) Weitere Beiträge zur Kenntnis der Gattung Graphiola. Ann Mycol 20:228–237
Google Scholar
Fischer GW, Holton CS (1957) Biology and control of the smut fungi. Ronald Press, New York
Google Scholar
Fonseca Á, Inácio J (2006) Phylloplane yeasts. In: Peter G, Rosa C (eds) Biodiversity and ecophysiology of yeasts. Springer, Berlin, pp 263–301
Google Scholar
Garcia-Muse T, Steinberg G, Perez-Martin J (2003) Pheromone-induced G2 arrest in the phytopathogenic fungus Ustilago maydis. Eurkaryot Cell 2:494–500. doi:10.1128/EC.2.3.494-500.2003
CAS Google Scholar
Gäumann E (1922) Über die Gattung Kordyana Rac. Ann Mycol 20:257–271
Google Scholar
Geiser E, Wierckx N, Zimmermann M, Blank LM (2013) Identification of an endo-1, 4-beta-xylanase of Ustilago maydis. BMC Biotechnol 13:59
CAS PubMed Central PubMed Google Scholar
Gerson U, Gafni A, Paz Z, Sztejnberg A (2008) A tale of three acaropathogenic fungi in Israel: Hirsutella, Meira and Acaromyces. Exp Appl Acarol 46:183–194
CAS PubMed Google Scholar
Goates BJ, Hoffmann JA (1986) Formation and discharge of secondary sporidia of the bunt fungus, Tilletia foetida. Mycologia 78:371–379
Google Scholar
Golubev WI (2006) Antagonistic interactions among yeasts. In: Peter G, Rosa C (eds) Biodiversity and ecophysiology of yeasts. Springer, Berlin, pp 197–219
Google Scholar
Golubev WI (2007) Mycocinogeny in smut yeast-like fungi of the genus Pseudozyma. Microbiology 76:719–722
CAS Google Scholar
Golubev WI, Kulakovskaya TV, Shashkov AS, Kulakovskaya EV, Golubev NV (2008) Antifungal cellobiose lipid secreted by the epiphytic yeast Pseudozyma graminicola. Microbiology 77:171–175
CAS Google Scholar
Gonzales V, Vánky K, Platas G, Lutz M (2007) Portalia gen. nov (Ustilaginomycotina). Fungal Divers 27:45–59
Google Scholar
Gottschalk M, Blanz PA (1985) Untersuchungen an 5S ribosomalen Ribonucleinsäuren als Beitrag zur Klärung von Systematik und Phylogenie der Basidiomyceten. Z Mycol 51:205–243
Google Scholar
Guého E, Boekhout T, Ashbee HR, Guillot J, Van Belkum A, Faergemann J (1998) The role of Malassezia species in the ecology of human skin and as pathogens. Med Mycol 36:220–229
PubMed Google Scholar
Guého-Kellermann E, Boekhout T, Begerow D (2010) Biodiversity, phylogeny and ultrastructure. In: Boekhout T, Guého E, Mayser P, Velegraki A (eds) Malassezia and the skin. Science and clinical practice. Springer, Berlin, pp 17–63
Google Scholar
Haslam E, Cai Y (1994) Plant polyphenols (vegetable tannins): gallic acid metabolism. Nat Prod Rep 11:41–66
CAS PubMed Google Scholar
Hawksworth DL (2011) A new dawn for the naming of fungi: impacts of decisions made in Melbourne in July 2011 on the future publication and regulation of fungal names. Mycokeys 1:7–20
Google Scholar
Hawksworth DL, Crous PW, Redhead SA, Reynolds DR, Samson RA, Seifert KA, Taylor JW, Wingfield MJ, Abaci Ö, Aime C, Asan A, Bai F-Y, de Beer ZW, Begerow D, Berikten D, Boekhout T, Buchanan PK, Burgess TI, Buzina W, Cai L, Cannon PF, Crane JL, Damm U, Daniel H-M, van Diepeningen AD, Druzhinina IS, Dyer PS, Eberhardt U, Fell JW, Frisvad JC, Geiser DM, Geml J, Glienke C, Gräfenhan T, Groenewald JZ, Groenewald M, de Gruyter JZ, Guého-Kellermann E, Hibbett DS, Hong S-B, de Hoog GS, Houbraken JAMP, Huhndorf SM, Hyde KD, Ismail A, Johnston PR, Kadaifciler DG, Kirk PM, Kõljalg U, Kurtzman CP, Lagneau P-E, Lévesque CA et al (2011) The Amsterdam Declaration on Fungal Nomenclature. IMA Fungus 2:105–112. doi:10.5598/imafungus.2011.02.01.14
PubMed Central PubMed Google Scholar
Hendrichs M, Bauer R, Oberwinkler F (2003) The Cryptobasidiaceae of tropical Central and South America. Sydowia 55:33–64
Google Scholar
Hendrichs M, Begerow D, Bauer R, Oberwinkler F (2005) The genus Anthracoidea (Basidiomycota, Ustilaginales): a molecular phylogenetic approach using LSU rDNA sequences. Mycol Res 109:31–40
CAS PubMed Google Scholar
Hennings P (1900) Exobasidiineae. In: Engler A, Prantl K (eds) Die natürlichen Pflanzenfamilien 1,1. Verlag von W. Engelmann, Leipzig, Germany, pp 103–105
Google Scholar
Hibbett DS, Binder M, Bischoff JF, Blackwell M, Cannon PF, Eriksson OE, Huhndorf S, James T, Kirk PM, Lucking R, Lumbsch TH, Lutzoni F, Matheny PB, McLaughlin DJ, Powell MJ, Redhead S, Schoch CL, Spatafora JW, Stalpers JA, Vilgalys R, Aime MC, Aptroot A, Bauer R, Begerow D, Benny GL, Castlebury LA, Crous PW, Dai YC, Gams W, Geiser DM, Griffith GW, Gueidan C, Hawksworth DL, Hestmark G, Hosaka K, Humber RA, Hyde KD, Ironside JE, Kõljalg U, Kurtzman CP, Larsson KH, Lichtwardt R, Longcore J, Miadlikowska J, Miller A, Moncalvo JM, Mozley-Standridge S, Oberwinkler F, Parmasto E, Reeb V, Rogers JD, Roux C, Ryvarden L, Sampaio P, Schussler A, Sugiyama J, Thorn RG, Tibell L, Untereiner WA, Walker C, Wang Z, Weir A, Weiss M, White MM, Winka K, Yao YJ, Zhang N (2007) A higher-level phylogenetic classification of the Fungi. Mycol Res 111:509–547
PubMed Google Scholar
Inácio J, Landell MF, Valente P, Wang PH, Wang YT, Yang SH, Manson JS, Lachance MA, Rosa CA, Fonseca Á (2008) Farysizyma gen. nov., an anamorphic genus in the Ustilaginales to accommodate three novel epiphytic basidiomycetous yeast species from America, Europe and Asia. FEMS Yeast Res 8:499–508
PubMed Google Scholar
Ingold CT (1983) The basidium in Ustilago. Trans Br Mycol Soc 81:573–584
Google Scholar
Ingold CT (1985) Dicellomyces scirpi: its conidial stage and taxonomic position. Trans Br Mycol Soc 84:542–545
Google Scholar
Ingold CT (1987a) Germination of teliospores in certain smuts. Trans Br Mycol Soc 88:355–363
Google Scholar
Ingold CT (1987b) Ballistospores and blastic conidia of Tilletia ayresii, and comparison with those of T. tritici and Entyloma ficariae. Trans Br Mycol Soc 88:75–82
Google Scholar
Ingold CT (1987c) Aerial sporidia of Ustilago hypodytes and Sorosporium saponariae. Trans Br Mycol Soc 89:471–475
Google Scholar
Ingold CT (1989a) Basidium development in some species of Ustilago. Mycol Res 93:405–412
Google Scholar
Ingold CT (1989b) Note on the basidium in the Tilletiaceae. Mycol Res 93:387–389
Google Scholar
Ingold CT (1989c) The basidium of Anthracoidea inclusa in relation to smut taxonomy. Mycol Res 92:245–246
Google Scholar
Ingold CT (1997) Teliospore germination in Tilletia opaca and T. sumatii and the nature of the tilletiaceous basidium. Mycol Res 101:281–284
Google Scholar
Ingold CT (1999) Two types of basidia in Urocystis hypoxis and the implications for smut taxonomy. Mycol Res 103:18–20
Google Scholar
Juarez-Montiel M, Ruiloba de Leon S, Chavez-Camarillo G, Hernandez-Rodriguez C, Villa-Tanaca L (2011) Huitlacoche (corn smut), caused by the phytopathogenic fungus Ustilago maydis, as a functional food. Rev Iberoam Micol 28:69–73. doi:10.1016/j.riam.2011.01.001
PubMed Google Scholar
Kahmann R, Kämper J (2004) Ustilago maydis: how its biology relates to pathogenic development. New Phytol 164:31–42
CAS Google Scholar
Kämper J, Kahmann R, Bölker M, Ma LJ, Brefort T, Saville BJ, Banuett F, Kronstad JW, Gold SE, Muller O, Perlin MH, Wosten HA, De Vries R, Ruiz-Herrera J, Reynaga-Pena CG, Snetselaar K, Mccann M, Perez-Martin J, Feldbrügge M, Basse CW, Steinberg G, Ibeas JI, Holloman W, Guzman P, Farman M, Stajich JE, Sentandreu R, Gonzalez-Prieto JM, Kennell JC, Molina L, Schirawski J, Mendoza-Mendoza A, Greilinger D, Munch K, Rossel N, Scherer M, Vranes M, Ladendorf O, Vincon V, Fuchs U, Sandrock B, Meng S, Ho EC, Cahill MJ, Boyce KJ, Klose J, Klosterman SJ, Deelstra HJ, Ortiz-Castellanos L, Li W, Sanchez-Alonso P, Schreier PH, Hauser-Hahn I, Vaupel M, Koopmann E, Friedrich G, Voss H, Schluter T, Margolis J, Platt D, Swimmer C, Gnirke A, Chen F, Vysotskaia V, Mannhaupt G, Guldener U, Munsterkotter M, Haase D, Oesterheld M, Mewes HW, Mauceli EW, Decaprio D, Wade CM, Butler J, Young S, Jaffe DB, Calvo S, Nusbaum C, Galagan J, Birren BW (2006) Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444:97–101
PubMed Google Scholar
Kellner R, Vollmeister E, Feldbrügge M, Begerow D (2011) Interspecific sex in grass smuts and the genetic diversity of their pheromone-receptor system. PLoS Genet 7:e1002436. doi:10.1371/journal.pgen.1002436
CAS PubMed Central PubMed Google Scholar
Kirk PM, Cannon PF, Minter DW, Stalpers JA (2008) Dictionary of fungi, 10th edn. CABI, Wallingford
Google Scholar
Kitamoto D, Yanagishita H, Shinbo T, Nakane T, Kamisawa C, Nakahara T (1993) Surface active properties and antimicrobial activities of mannosylerythritol lipids as biosurfactants produced by Candida antarctica. J Biotechnol 29:91–96
CAS Google Scholar
Kochman J (1939) Beitrag zur Kenntnis der Brandpilzflora Polens II. Acta Soc Bot Pol 16:53–67
Google Scholar
Kreisel H (1969) Grundzüge eines natürlichen Systems der Pilze. Cramer, Vaduz
Google Scholar
Kukkonen I, Raudaskoski M (1964) Studies on the probable homothallism and pseudohomothallism in the genus Anthracoidea. Ann Bot Fenn 1:257–271
Google Scholar
Kurtzman CP, Fell JW, Boekhout T (2011) The yeasts: a taxonomic study. Elsevier, London
Google Scholar
Kurtzman CP, Sugiyama J (2014) Taphrinomycotina and Saccharomycotina. In: McLaughlin DJ, Spatafora JW (eds) The Mycota, vol. 7B, 2nd edn, Systematics and evolution. Springer, Berlin
Google Scholar
Kushnir L, Paz Z, Gerson U, Sztejnberg A (2011) The effect of three basidiomycetous fungal species on soil-borne, foliage and fruit-damaging phytopathogens in laboratory experiments. BioControl 56:799–810
CAS Google Scholar
Lendner A (1920) Un champignon parasite sur une Lauracée du genre Ocotea. Bull Soc Bot Genève 12:122–128
Google Scholar
Lin SS, Pranikoff T, Smith SF, Brandt ME, Gilbert K, Palavecino EL, Shetty AK (2008) Central venous catheter infection associated with Pseudozyma aphidis in a child with short gut syndrome. J Med Microbiol 57:516–518
PubMed Google Scholar
Liou GY, Wei YH, Lin SJ, Wen CY, Lee FL (2009) Pseudozyma pruni sp. nov., a novel ustilaginomycetous anamorphic fungus from flowers in Taiwan. Int J Syst Evol Microbiol 59:1813–1817
CAS PubMed Google Scholar
Luttrell ES (1987) Relations of hyphae to host cells in smut galls caused by species of Tilletia, Tolyposporium, and Ustilago. Can J Bot 65:2581–2591
Google Scholar
Lutz M, Vánky K, Bauer R (2011) Melanoxa, a new genus in the Urocystidales (Ustilaginomycotina). Mycol Prog 11:149–158. doi:10.1007/s11557-010-0737-7
Google Scholar
Lutz M, Vánky K, Piątek M (2012) Shivasia gen. nov. for the Australasian smut Ustilago solida that historically shifted through five different genera. IMA Fungus 3:143–154
PubMed Central PubMed Google Scholar
Mahdi LE, Statzell-Tallman A, Fell JW, Brown MV, Donachie SP (2008) Sympodiomycopsis lanaiensis sp. nov., a basidiomycetous yeast (Ustilaginomycotina: Microstromatales) from marine driftwood in Hawai’i. FEMS Yeast Res 8:1357–1363
CAS PubMed Central PubMed Google Scholar
Malençon G (1953) Le Coniodyctium chevalieri Har. et Pat., sa nature et ses affinitiés. Bull Soc Myc Fr 69:77–100
Google Scholar
Matheny PB, Gossmann JA, Zalar P, Kumar TKA, Hibbett DS (2006) Resolving the phylogenetic position of the Wallemiomycetes: an enigmatic major lineage of Basidiomycota. Can J Bot 84:1794–1805
CAS Google Scholar
Mathre DE (1996) Dwarf bunt: politics, identification, and biology. Annu Rev Phytopathol 34:67–85
CAS PubMed Google Scholar
Maublanc MA (1914) Les genres Drepanoconis Schr. et Henn. et Clinoconidium Pat.: leur structure et leur place dans la classification. Bull Soc Myc Fr 30:444–446
Google Scholar
McTaggart AR, Shivas RG, Geering ADW, Callaghan B, Vánky K, Scharaschkin T (2012a) Soral synapomorphies are significant for the systematics of the Ustilago-Sporisorium-Macalpinomyces complex (Ustilaginaceae). Persoonia 29:63–77
CAS PubMed Central PubMed Google Scholar
McTaggart AR, Shivas RG, Geering ADW, Vánky K, Scharaschkin T (2012b) A review of the Ustilago-Sporisorium-Macalpinomyces complex. Persoonia 29:55–62
CAS PubMed Central PubMed Google Scholar
McTaggart AR, Shivas RG, Geering ADW, Vánky K, Scharaschkin T (2012c) Taxonomic revision of Ustilago, Sporisorium and Macalpinomyces. Persoonia 29:116–132
CAS PubMed Central PubMed Google Scholar
Mimee B, Labbé C, Pelletier R, Bélanger RR (2005) Antifungal activity of flocculosin, a novel glycolipid isolated from Pseudozyma flocculosa. Antimicrob Agents Chemother 49:1597–1599
CAS PubMed Central PubMed Google Scholar
Mims CW, Richardson EA (2007) Light and electron microscopic observation of the infection of Camellia sasanqua by the fungus Exobasidium camelliae var. gracilis. Can J Bot 85:175–183
Google Scholar
Mims CW, Snetselaar KM (1991) Teliospore maturation in the smut fungus Sporisorium sorghi: an ultrastructural study using freeze substitution fixation. Bot Gaz 152:1–7
Google Scholar
Mims CW, Richardson EA, Roberson RW (1987) Ultrastructure of basidium and basidiospore development in three species of the fungus Exobasidium. Can J Bot 65:1236–1244
Google Scholar
Mims CW, Snetselaar KM, Richardson EA (1992) Ultrastructure of the leaf stripe smut fungus Ustilago striiformis: host-pathogen relationship and teliospore development. Int J Plant Sci 153:289–290
Google Scholar
Müller B (1989) Chemotaxonomische Untersuchungen an Basidiomycetenhefen. Thesis, University of Tübingen, Tübingen, Germany
Google Scholar
Nagler A (1986) Untersuchungen zur Gattungsabgrenzung von Ginanniella Ciferri und Urocystis Rabenhorst sowie zur Ontogenie von Thecaphora seminis-convolvuli (Desm.) Ito. Thesis, University of Tübingen, Tübingen, Germany
Google Scholar
Nagler A, Bauer R, Berbee M, Vánky K, Oberwinkler F (1989) Light and electron microscopic studies of Schroeteria delastrina and S. poeltii. Mycologia 81:884–895
Google Scholar
Nannfeldt JA (1981) Exobasidium, a taxonomic reassessment applied to the European species. Symb Bot Upsal 23:1–71
Google Scholar
Oberwinkler F (1977) Das neue System der Basidiomyceten. In: Frey W, Hurka H, Oberwinkler F (eds) Beiträge zur Biologie der niederen Pflanzen. Gustav Fischer, Stuttgart, pp 59–105
Google Scholar
Oberwinkler F (1978) Was ist ein Basidiomycet? Z Mykol 44:13–29
Google Scholar
Oberwinkler F (1982) The significance of the morphology of the basidium in the phylogeny of basidiomycetes. In: Wells K, Wells EK (eds) Basidium and basidiocarp. Springer, Berlin, Heidelberg, New York, pp 9–35
Google Scholar
Oberwinkler F (1985) Zur Evolution und Systematik der Basidiomyceten. Bot Jahrb Syst 107:541–580
Google Scholar
Oberwinkler F (1987) Heterobasidiomycetes with ontogenetic yeast stages-systematic and phylogenetic aspects. Stud Mycol 30:61–74
Google Scholar
Oberwinkler F (1993) Diversity and phylogenetic importance of tropical heterobasidiomycetes. In: Isaac S, Frankland JC, Watling R, Whalley AJS (eds) Aspects of tropical mycology. Cambridge University Press, Cambridge, UK, pp 121–147
Google Scholar
Oberwinkler F, Bandoni RJ, Blanz P, Deml G, Kisimova-Horovitz L (1982) Graphiolales: basidiomycetes parasitic on palms. Plant Systemat Evol 140:251–277
Google Scholar
Olive LS (1945) A new Dacrymyces-like parasite of Arundinaria. Mycologia 37:543–552
Google Scholar
Pascoe IG, Priest MJ, Shivas RG, Cunnington JH (2005) Ustilospores of Tilletia ehrhartae, a smut of Ehrharta calycina, are common contaminants of Australian wheat grain, and potential source of confusion with Tilletia indica, the cause of Karnal bunt of wheat. Plant Pathol 54:161–168
Google Scholar
Patil MS (1977) A new species of Muribasidiospora from Kolhapur. Kavaka 5:31–33
Google Scholar
Paz Z, Burdman S, Gerson U, Sztejnberg A (2007) Antagonistic effects of the endophytic fungus Meira geulakonigii on the citrus rust mite Phyllocoptruta oleivora. J Appl Microbiol 103:2570–2579
CAS PubMed Google Scholar
Pegg GS, Webb RI, Carnegie AJ, Wingfield MJ, Drenth A (2009) Infection and disease development of Quambalaria spp. on Corymbia and Eucalyptus species. Plant Pathol 58:642–654
Google Scholar
Piątek M, Vánky K, Mossebo DC, Piątek J (2008) Doassansiopsis caldesiae sp. nov. and Doassansiopsis tomasii: two remarkable smut fungi from Cameroon. Mycologia 100:662–672
PubMed Google Scholar
Piepenbring M, Bauer R (1995) Noteworthy germinations of some Costa Rican Ustilaginales. Mycol Res 99:853–858
Google Scholar
Piepenbring M, Bauer R (1997) Erratomyces, a new genus of Tilletiales with species on Leguminosae. Mycologia 89:924–936
Google Scholar
Piepenbring M, Bauer R, Oberwinkler F (1998) Teliospores of smut fungi: general aspects of teliospore walls and sporogenesis. Protoplasma 204:155–169
Google Scholar
Piepenbring M, Espinoza J, Saldana L, Caceres O (2010) New records, host plants, morphological and molecular data of Exobasidiales (Basidiomycota) from Panama. Nova Hedwigia 19:231–242. doi:10.1127/0029-5035/2010/0091-0231
Google Scholar
Posada F, Vega FE (2005) Coffee endophytes pathogenic to the coffee berry borer. In: 38th annual meeting of the society for invertebrate pathology, program and abstracts, 7–11 Aug 2005, Anchorage, AK
Google Scholar
Preece TF, Hick AJ (2001) An introduction to the Protomycetales: Burenia inundata on Apium nodiflorum and Protomyces macrosporus on Anthriscus sylvestris. Mycologist 15:119–125
Google Scholar
Prillinger H, Dörfler C, Laaser G, Hauska G (1990) Ein Beitrag zur Systematik und Entwicklungsbiologie höherer Pilze. Hefe-Typen der Basidiomyceten. Teil III. Ustilago-Typ. Z Mykol 56:251–278
Google Scholar
Prillinger H, Deml G, Dörfler C, Laaser G, Lockau W (1991) Ein Beitrag zur Systematik und Entwicklungsbiologie höherer Pilze: Hefe-Typen der Basidiomyceten. Teil II. Microbotryum-Typ. Bot Acta 104:5–17
CAS Google Scholar
Prillinger H, Oberwinkler F, Umile C, Tlachac K, Bauer R, Dörfler C, Taufratzhofer E (1993) Analysis of cell wall carbohydrates (neutral sugars) from ascomycetous and basidiomycetous yeasts with and without derivatization. J General Appl Microbiol 39:1–34
CAS Google Scholar
Rajendren RB (1968) Muribasidiospora-a new genus of the Exobasidiaceae. Mycopathologia 36:218–222
Google Scholar
Reddy MS, Kramer CL (1975) A taxonomic revision of the Protomycetales. Mycotaxon 3:1–50
Google Scholar
Ritschel A, Begerow D, Oberwinkler F (2008) A new species of Volvocisporium from Namibia, V. grewiae sp. nov. (Microstromatales, Ustilaginomycota). Mycol Prog 7:1–5
Google Scholar
Roberson RW, Luttrell ES (1987) Ultrastructure of teliospore ontogeny in Tilletia indica. Mycologia 79:753–763
Google Scholar
Roberson RW, Luttrell ES (1989) Dolipore septa in Tilletia. Mycologia 81:650–652
Google Scholar
Roets F, Dreyer LL, Wingfield MJ, Begerow D (2008) Thecaphora capensis sp. nov., an unusual new anther smut on Oxalis in South Africa. Persoonia 21:47–152
Google Scholar
Rush TA, Aime MC (2013) The genus Meira: phylogenetic placement and description of a new species. Antonie Van Leeuwenhoek 103:1–10
Google Scholar
Sampaio JP (1999) Utilization of low molecular weight aromatic compounds by heterobasidiomycetous yeasts: taxonomic implications. Can J Microbiol 45:491–512
CAS PubMed Google Scholar
Sampaio JP (2004) Diversity, phylogeny and classification of basidiomycetous yeasts. In: Agerer R, Piepenbring M, Blanz P (eds) Frontiers in basidiomycote mycology. IHW, Eching, Germany, pp 49–80
Google Scholar
Sampson K (1939) Life cycles of smut fungi. Trans Br Mycol Soc 23:1–23
Google Scholar
Savchenko KG, Lutz M, Piątek M, Heluta VP, Nevo E (2013) Anthracoidea caricis-meadii is a new North American smut fungis Carex sect. Paniceae. Mycologia 105:181–193
PubMed Google Scholar
Savile DBO (1947) A study of the species of Entyloma on North American composites. Can J Res 25:105–120
Google Scholar
Schäfer AM, Kemler M, Bauer R, Begerow D (2010) The illustrated life cycle of Microbotryum on the host plant Silene latifolia. Can J Bot 88:875–885
Google Scholar
Scherer M, Heimel K, Starke V, Kämper J (2006) The Clp1 protein is required for clamp formation and pathogenic development of Ustilago maydis. Plant Cell 18:2388–2401
CAS PubMed Central PubMed Google Scholar
Schirawski J, Böhnert HU, Steinberg G, Snetselaar K, Adamikowa L, Kahmann R (2005) Endoplasmic reticulum glucosidase II is required for pathogenicity of Ustilago maydis. Plant Cell 17:3532–3543
CAS PubMed Central PubMed Google Scholar
Schirawski J, Mannhaupt G, Münch K, Brefort T, Schipper K, Doehlemann G, Di Stasio M, Rössel N, Mendoza-Mendoza A, Pester D, Müller O, Winterberg B, Meyer E, Ghareeb H, Wollenberg T, Münsterkötter M, Wong P, Walter M, Stukenbrock E, Güldener U, Kahmann R (2010) Pathogenicity determinants in smut fungi revealed by genome comparison. Science 330:1546–1548. doi:10.1126/science.1195330
CAS PubMed Google Scholar
Schröter J (1894) Uleiella gen. nov. In: Pazschke, Sammlungen. Hedwigia Beibl 33:64–66
Google Scholar
Seo HS, Um HJ, Min J, Rhee SK, Cho TJ, Kim YH, Lee J (2007) Pseudozyma jejuensis sp. nov., a novel cutinolytic ustilaginomycetous yeast species that is able to degrade plastic waste. FEMS Yeast Res 7:1035–1045
CAS PubMed Google Scholar
Shivas RG (2009) Three new species of Tilletia on native grasses from Australia. Australas Plant Pathol 38:128–131
Google Scholar
Singh RA, Pavgi MS (1973) Morphology, cytology and development of Melanotaenium brachiariae. Cytologia 38:455–466
Google Scholar
Sipiczki M, Kajdacsi E (2009) Jaminaea angkorensis gen. nov., sp. nov., a novel anamorphic fungus containing an S943 nuclear small-subunit rRNA group IB intron represents a basal branch of Microstromatales. Int J Syst Evol Microbiol 59:914–920
CAS PubMed Google Scholar
Skibbe DS, Doehlemann G, Fernandes J, Walbot V (2010) Maize tumors caused by Ustilago maydis require organ-specific genes in host and pathogen. Science 328:89. doi:10.1126/science.1185775
CAS PubMed Google Scholar
Snetselaar KM, Mims CW (1992) Sporidial fusion and infection of maize seedlings by the smut fungus Ustilago maydis. Mycologia 84:193–203
Google Scholar
Snetselaar KM, Mims CW (1994) Light and electron microscopy of Ustilago maydis hyphae in maize. Mycol Res 98:347–355
Google Scholar
Snetselaar KM, Tiffany LH (1990) Light and electron microscopy of sorus development in Sorosporium provinciale, a smut of big bluestem. Mycologia 82:480–492
Google Scholar
Stoll M, Piepenbring M, Begerow D, Oberwinkler F (2003) Molecular phylogeny of Ustilago and Sporisorium species (Basidiomycota, Ustilaginales) based on internal transcribed spacer (ITS) sequences. Can J Bot 81:976–984
CAS Google Scholar
Stoll M, Begerow D, Oberwinkler F (2005) Molecular phylogeny of Ustilago, Sporisorium, and related taxa based on combined analyses of rDNA sequences. Mycol Res 109:342–356
CAS PubMed Google Scholar
Subba Rao PV, Fritig B, Vose JR, Towers GHN (1971) An aromatic 3,4-oxygenase from Tilletiopsis washingtonensis—oxidation of 3,4-dihydroxyphenylacetic acid to β-carboxymethylmuconolactone. Phytochemistry 10:51–56
Google Scholar
Sugita T, Takashima M, Poonwan N, Mekha N, Malaithao K, Thungmuthasawat B, Prasarn S, Luangsook P, Kudo T (2003) The first isolation of ustilaginomycetous anamorphic yeasts, Pseudozyma species, from patients blood and a description of two new species: P. parantarctica and P. thailandica. Microbiol Immunol 47:183–190
CAS PubMed Google Scholar
Sugiyama J, Hosaka K, Suh SO (2006) Early diverging Ascomycota: phylogenetic divergence and related evolutionary enigmas. Mycologia 98:996–1005. doi:10.3852/mycologia.98.6.996
PubMed Google Scholar
Sundström KR (1964) Studies of the physiology, morphology and serology of Exobasidium. Symb Bot Ups 18:3, 89 p
Google Scholar
Swann EC, Taylor JW (1993) Higher taxa of basidiomycetes: an 18S rRNA gene perspective. Mycologia 85:923–936
CAS Google Scholar
Swann EC, Taylor JW (1995) Phylogenetic diversity of yeast-producing basidiomycetes. Mycol Res 99:1205–1210
Google Scholar
Sydow H (1926) Fungi in itinere costaricensi collecti. Pars secunda. Ann Mycol 24:283–288
Google Scholar
Takahashi H, Sekiguchi H, Ito T, Sasahara M, Hatanaka N, Ohba A, Hase S, Ando S, Hasegawa H, Takenaka S (2011) Microbial community profiles in intercellular fluid of rice. J Gen Plant Pathol 77:121–131
CAS Google Scholar
Tanaka E, Shimizu K, Imanishi Y, Yasuda F, Tanaka C (2008) Isolation of basidiomycetous anamorphic yeast-like fungus Meira argovae found on Japanese bamboo. Mycoscience 49:329–333
Google Scholar
Taylor JW, Berbee ML (2006) Dating divergences in the Fungal Tree of Life: review and new analyses. Mycologia 98:838–849
PubMed Google Scholar
Teichmann B, Linne U, Hewald S, Marahiel MA, Bölker M (2007) A biosynthetic gene cluster for a secreted cellobiose lipid with antifungal activity from Ustilago maydis. Mol Microbiol 66:525–533
CAS PubMed Google Scholar
Thomas PL (1989) Barley smuts in the prairie provinces of Canada, 1983-1988. Can J Phytopathol 11:133–136
Google Scholar
Trail F, Mills D (1990) Growth of haploid Tilletia strains in planta and genetic analysis of a cross of Tilletia caries X Tilletia controversa. Phytopathology 80:367–370
Google Scholar
Trindade RC, Resende MA, Silva CM, Rosa CA (2002) Yeasts associated with fresh and frozen pulps of Brazilian tropical fruits. Syst Appl Microbiol 25:294–300
CAS PubMed Google Scholar
Trione EJ (1982) Dwarf bunt of wheat and its importance in international wheat trade. Plant Dis 66:1083–1088
Google Scholar
Trione EJ, Hess WM, Stockwell VO (1989) Growth and sporulation of the dikaryons of the dwarf bunt fungus in wheat plants and in culture. Can J Bot 67:1671–1680
Google Scholar
Tulasne L, Tulasne C (1847) Mémoire sur les Ustilaginées comparées Uredinées. Ann Sci Nat Bot 3:12–127
Google Scholar
Urquhart EJ, Punja ZK (2002) Hydrolytic enzymes and antifungal compounds produced by Tilletiopsis species, phyllosphere yeasts that are antagonists of powdery mildew fungi. Can J Microbiol 48:219–229
CAS PubMed Google Scholar
Valverde ME, Paredes-Lópes O, Pataky JK, Guevara-Lara F (1995) Huitlacoche (Ustilago maydis) as a food source—biology, composition, and production. CRC Crit Rev Food Sci Nutr 35:191–229
CAS Google Scholar
Vánky K (1981) The genus Schroeteria Winter (Ustilaginales). Sydowia 34:157–166
Google Scholar
Vánky K (1987) Illustrated genera of smut fungi. Cryptogam Stud 1:1–159
Google Scholar
Vánky K (1994) European smut fungi. Gustav Fischer, Stuttgart
Google Scholar
Vánky K (1996) Mycosyrinx and other pair-spored Ustilaginales. Mycoscience 37:173–185
Google Scholar
Vánky K (2000) New taxa of Ustilaginomycetes. Mycotaxon 74:343–356
Google Scholar
Vánky K (2001) The emended Ustilaginaceae of the modern classificatory system for smut fungi. Fungal Divers 6:131–147
Google Scholar
Vánky K (2003) Cintractiellaceae fam. nov. (Ustilaginomycetes). Fungal Divers 13:167–173
Google Scholar
Vánky K (2005) The smut fungi (Ustilaginomycetes) of Eriocaulaceae. I. Eriomoeszia gen. nov. Mycol Balc 2:105–111
Google Scholar
Vánky K (2011) The genus Pericladium (Ustilaginales). Pericladiaceae fam. nov. Mycol Balc 8:147–152
Google Scholar
Vánky K (2012) Smut fungi of the world. APS, St. Paul, MN
Google Scholar
Vánky K, Bauer R (1992) Conidiosporomyces, a new genus of Ustilaginales. Mycotaxon 43:426–435
Google Scholar
Vánky K, Bauer R (1995) Oberwinkleria, a new genus of Ustilaginales. Mycotaxon 53:361–368
Google Scholar
Vánky K, Bauer R (1996) Ingoldiomyces, a new genus of Ustilaginales. Mycotaxon 59:277–287
Google Scholar
Vánky K, Lutz M (2011) Tubisorus, a new genus of smut fungi (Ustilaginomycetes) for Sorosporium pachycarpum. Mycol Blac 8:129–135
Google Scholar
Vánky K, Bauer R, Begerow D (1998) Doassinga, a new genus of Doassansiales. Mycologia 90:964–970
Google Scholar
Vánky K, Lutz M, Shivas RG (2006) Anomalomyces panici, new genus and species of Ustilaginomycetes from Australia. Mycol Balc 3:119–126
Google Scholar
Vánky K, Lutz M, Bauer R (2007) Revision of some Thecaphora species (Ustilaginomycotina) on Caryophyllaceae. Mycol Res 111:1207–1219
PubMed Google Scholar
Vánky K, Lutz M, Bauer R (2008a) About the genus Thecaphora (Glomosporiaceae) and its new synonyms. Mycol Prog 7:31–39
Google Scholar
Vánky K, Lutz M, Bauer R (2008b) Floromyces, a new genus of Ustilaginomycotina. Mycotaxon 104:171–184
Google Scholar
Vishniac HS (2006) A multivariate analysis of soil yeasts isolated from a latitudinal gradient. Microb Ecol 52:90–103
PubMed Google Scholar
Vishniac HS, Anderson JA, Filonow AB (1997) Assimilation of volatiles from ripe apples by Sporidiobolus salmonicolor and Tilletiopsis washingtonensis. Antonie Van Leeuwenhoek 72:201–207
CAS PubMed Google Scholar
Vollmeister E, Schipper K, Baumann S, Haag C, Pohlmann T, Stock J, Feldbrügge M (2012) Fungal development of the plant pathogen Ustilago maydis. FEMS Microbiol Rev 36:59–77. doi:10.1111/j.15746976.2011.00296.x
CAS PubMed Google Scholar
Wang QM, Jia JH, Bai FY (2006) Pseudozyma hubeiensis sp. nov. and Pseudozyma shanxiensis sp. nov., novel ustilaginomycetous anamorphic yeast species from plant leaves. Int J Syst Evol Microbiol 56:289–293
CAS PubMed Google Scholar
Wells K (1994) Jelly fungi, then and now! Mycologia 86:18–48
Google Scholar
Whitehead T (1921) On the life history and morphology of Urocystis cepulae. Trans Br Mycol Soc 7:65–71, plate II
Google Scholar
Xu J, Saunders CW, Hu P, Grant RA, Boekhout T, Kuramae EE, Kronstad JW, DeAngelis YM, Reeder NL, Johnstone KR, Leland M, Fieno AM, Begley WM, Sun Y, Lacey MP, Chaudhary T, Keough T, Chu L, Sears R, Yuan B, Dawson TL (2007) Dandruff-associated Malassezia genomes reveal convergent and divergent virulence traits shared with plant and human fungal pathogens. Proc Natl Acad Sci USA 104:18730–18735
CAS PubMed Central PubMed Google Scholar
Yasuda F, Yamagishi D, Hajime Akamatsu H, Izawa H, Kodama M, Otani H (2006) Meira nashicola sp. nov., a novel basidiomycetous, anamorphic yeastlike fungus isolated from Japanese pear fruit with reddish stain. Mycoscience 47:36–40
CAS Google Scholar
Zepeda L (2006) The Huitlacoche project: a tale of smut and gold. Renew Agr Food Syst 21:224–226. doi:10.1079/RAF2006153
Google Scholar
Zundel GL (1945) A change in generic name. Mycologia 37:795–796
Google Scholar

Download references

Acknowledgements

We thank Alistair McTaggart (Agri-Science Queensland, Australia) for his critical reading of the manuscript, Lori Carris (Washington State University, USA) and Hans Henrik Bruun (Center for Macroecology, Evolution and Climate, Denmark) for providing photographs of T. controversa and M. endogenum for Fig. 11.1, and Meike Piepenbring (Goethe Universität, Germany) for several drawings for Fig. 11.3. Kálmán Vánky (HUV, Germany) is acknowledged for many specimens and the Deutsche Forschungsgemeinschaft for financial support.

Author information

Authors and Affiliations

Ruhr-Universität Bochum, Geobotanik, ND 03/174, 44801, Bochum, Germany
D. Begerow & A. M. Schäfer
Max Planck Institute for Terrestrial Microbiology, Karl von Frisch Strasse 10, 35043, Marburg, Germany
R. Kellner
Leibniz Institute DSMZ-German Collection of Microorganisms and Cell Cultures, Inhoffenstraße 7B, 38124, Braunschweig, Germany
A. Yurkov
Centre of Excellence in Tree Health Biotechnology, Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria, 0002, South Africa
M. Kemler
Organismische Botanik, Universität Tübingen, Auf der Morgenstelle 1, 72076, Tübingen, Germany
F. Oberwinkler & R. Bauer

Authors

D. Begerow
View author publications
You can also search for this author in PubMed Google Scholar
A. M. Schäfer
View author publications
You can also search for this author in PubMed Google Scholar
R. Kellner
View author publications
You can also search for this author in PubMed Google Scholar
A. Yurkov
View author publications
You can also search for this author in PubMed Google Scholar
M. Kemler
View author publications
You can also search for this author in PubMed Google Scholar
F. Oberwinkler
View author publications
You can also search for this author in PubMed Google Scholar
R. Bauer
View author publications
You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to D. Begerow .

Editor information

Editors and Affiliations

Dept. Plant Biology, University of Minesota, St. Paul, Minnesota, USA
David J. McLaughlin
Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon, USA
Joseph W. Spatafora

Rights and permissions

Reprints and permissions

Copyright information

About this chapter

Cite this chapter

Begerow, D. et al. (2014). 11 Ustilaginomycotina . In: McLaughlin, D., Spatafora, J. (eds) Systematics and Evolution. The Mycota, vol 7A. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-55318-9_11

Download citation

DOI: https://doi.org/10.1007/978-3-642-55318-9_11
Published: 02 July 2014
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-55317-2
Online ISBN: 978-3-642-55318-9
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)

Publish with us

Policies and ethics